ROS homeostasis during development: an evolutionary conserved strategy

Abstract

The balance between cellular proliferation and differentiation is a key aspect of development in multicellular organisms. Recent studies on Arabidopsis roots revealed distinct roles for different reactive oxygen species (ROS) in these processes. Modulation of the balance between ROS in proliferating cells and elongating cells is controlled at least in part at the transcriptional level. The effect of ROS on proliferation and differentiation is not specific for plants but appears to be conserved between prokaryotic and eukaryotic life forms. The ways in which ROS is received and how it affects cellular functioning is discussed from an evolutionary point of view. The different redox-sensing mechanisms that evolved ultimately result in the activation of gene regulatory networks that control cellular fate and decision-making. This review highlights the potential common origin of ROS sensing, indicating that organisms evolved similar strategies for utilizing ROS during development, and discusses ROS as an ancient universal developmental regulator.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    PubMed  CAS  Google Scholar 

  2. 2.

    Halliwell B, Whiteman M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142:231–255

    PubMed  CAS  Google Scholar 

  3. 3.

    Hedges SB, Blair JE, Venturi ML, Shoe JL (2004) A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 4:2

    PubMed  Google Scholar 

  4. 4.

    Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tyryshkin A (2001) The origin of atmospheric oxygen on earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98:2170–2175

    PubMed  CAS  Google Scholar 

  5. 5.

    Falkowski PG (2006) Evolution: tracing oxygen’s imprint on earth’s metabolic evolution. Science 311:1724–1725

    PubMed  CAS  Google Scholar 

  6. 6.

    Danovaro R, Dell’Anno A, Pusceddu A, Gambi C, Heiner I, Kristensen RM (2010) The first metazoa living in permanently anoxic conditions. BMC Biol 6(8):30

    Google Scholar 

  7. 7.

    Knoll AH (2003) The geological consequences of evolution. Geobiology 1:3–14

    CAS  Google Scholar 

  8. 8.

    Raymond J, Segrè D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767

    PubMed  CAS  Google Scholar 

  9. 9.

    Nealson KH, Conrad PG (1999) Life: past, present and future. Philos Trans R Soc Lond B 354:1923–1939

    CAS  Google Scholar 

  10. 10.

    Thannickal VJ (2009) Oxygen in the evolution of complex life and the price we pay. Am J Respir Cell Mol Biol 40:507–510

    PubMed  CAS  Google Scholar 

  11. 11.

    Rees DC, Howard JB (2003) The interface between the biological and inorganic worlds: iron-sulfur metalloclusters. Science 300:929–931

    PubMed  CAS  Google Scholar 

  12. 12.

    Outten FW (2007) Iron-sulfur clusters as oxygen-responsive molecular switches. Nat Chem Biol 3:206–267

    PubMed  CAS  Google Scholar 

  13. 13.

    Schippers JHM, Nunes-Nesi A, Apetrei R, Hille J, Fernie AR, Dijkwel PP (2008) The Arabidopsis onset of leaf death5 mutation of quinolinate synthase affects nicotinamide adenine dinucleotide biosynthesis and causes early ageing. Plant Cell 20:2909–2925

    PubMed  CAS  Google Scholar 

  14. 14.

    Lill R (2009) Function and biogenesis of iron–sulphur proteins. Nature 460:831–838

    PubMed  CAS  Google Scholar 

  15. 15.

    Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23:855–864

    PubMed  Google Scholar 

  16. 16.

    Kennedy KA, Sandiford SD, Skerjanc IS, Li SS (2012) Reactive oxygen species and the neuronal fate. Cell Mol Life Sci 69:215–221

    PubMed  CAS  Google Scholar 

  17. 17.

    Horke S, Witte I, Altenhöfer S, Wilgenbus P, Goldeck M, Förstermann U, Xiao J, Kramer GL, Haines DC, Chowdhary PK, Haley RW, Teiber JF (2009) Paraoxonase 2 is down-regulated by the Pseudomonas aeruginosa quorumsensing signal N-(3-oxododecanoyl)-l-homoserine lactone and attenuates oxidative stress induced by pyocyanin. Biochem J 426:73–83

    Google Scholar 

  18. 18.

    Thön M, Al-Abdallah Q, Hortschansky P, Brakhage AA (2007) The thioredoxin system of the filamentous fungus Aspergillus nidulans: impact on development and oxidative stress response. J Biol Chem 282:27259–27269

    PubMed  Google Scholar 

  19. 19.

    Bloomfield G, Pears C (2003) Superoxide signalling required for multicellular development of Dictyostelium. J Cell Sci 116:3387–3397

    PubMed  CAS  Google Scholar 

  20. 20.

    Faulkner MJ, Ma Z, Fuangthong M, Helmann JD (2012) Derepression of the Bacillus subtilis PerR peroxide stress response leads to iron deficiency. J Bacteriol 194:1226–1235

    PubMed  CAS  Google Scholar 

  21. 21.

    Zheng M, Aslund F, Storz G (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718–1721

    PubMed  CAS  Google Scholar 

  22. 22.

    Giedroc DP (2009) Hydrogen peroxide sensing in Bacillus subtilis: it is all about the (metallo) regulator. Mol Microbiol 73:1–4

    PubMed  CAS  Google Scholar 

  23. 23.

    Hidalgo E, Ding H, Demple B (1997) Redox signal transduction via iron-sulfur clusters in the SoxR transcription activator. Trends Biochem Sci 22:207–210

    PubMed  CAS  Google Scholar 

  24. 24.

    Delaunay A, Isnard AD, Toledano MB (2000) H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19:5157–5166

    PubMed  CAS  Google Scholar 

  25. 25.

    Moi P, Chan K, Asunis I, Cao A, Kan YW (1994) Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci USA 91:9926–9930

    PubMed  CAS  Google Scholar 

  26. 26.

    Reddy NM, Kleeberger SR, Yamamoto M, Kensler TW, Scollick C, Biswal S, Reddy SP (2007) Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiol Genomics 32:74–81

    PubMed  CAS  Google Scholar 

  27. 27.

    Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    PubMed  CAS  Google Scholar 

  28. 28.

    Fobert PR, Després C (2005) Redox control of systemic acquired resistance. Curr Opin Plant Biol 8:378–382

    PubMed  CAS  Google Scholar 

  29. 29.

    Garretón V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516–1526

    PubMed  Google Scholar 

  30. 30.

    Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    PubMed  CAS  Google Scholar 

  31. 31.

    Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol. doi:10.1016/j.pbi.2012.02.003

    PubMed  Google Scholar 

  32. 32.

    Ransone LJ, Verma IM (1990) Nuclear proto-oncogenes fos and jun. Annu Rev Cell Biol 6:539–557

    PubMed  CAS  Google Scholar 

  33. 33.

    Murphy LO, Smith S, Chen RH, Fingar DC, Blenis J (2002) Molecular interpretation of ERK signal duration by immediate early gene products. Nat Cell Biol 4:556–564

    PubMed  CAS  Google Scholar 

  34. 34.

    Tena G, Boudsocq M, Sheen J (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14:519–529

    PubMed  CAS  Google Scholar 

  35. 35.

    Boyce KJ, Andrianopoulos A (2011) Ste20-related kinases: effectors of signaling and morphogenesis in fungi. Trends Microbiol 19:400–410

    PubMed  CAS  Google Scholar 

  36. 36.

    Becatti M, Taddei N, Cecchi C, Nassi N, Nassi PA, Fiorillo C (2012) SIRT1 modulates MAPK pathways in ischemic-reperfused cardiomyocytes. Cell Mol Life Sci. doi:10.1007/s00018-012-0925-5

    PubMed  Google Scholar 

  37. 37.

    Thomason P, Kay R (2000) Eukaryotic signal transduction via histidine-aspartate phosphorelay. J Cell Sci 113:3141–3150

    PubMed  CAS  Google Scholar 

  38. 38.

    West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369–376

    PubMed  CAS  Google Scholar 

  39. 39.

    Parkinson JS (1993) Signal transduction schemes of bacteria. Cell 73:857–871

    PubMed  CAS  Google Scholar 

  40. 40.

    Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC, Saito H (1996) Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 “two-component” osmosensor. Cell 86:865–875

    PubMed  CAS  Google Scholar 

  41. 41.

    Yamada H, Hanaki N, Imamura A, Ueguchi C, Mizuno T (1998) An Arabidopsis protein that interacts with the cytokinin-inducible response regulator, ARR4, implicated in the His–Asp phosphorylay signal transduction. FEBS Lett 436:76–80

    PubMed  CAS  Google Scholar 

  42. 42.

    Wurgler-Murphy SM, Saito H (1997) Two-component signal transducers and MAPK cascades. Trends Biochem Sci 22:172–176

    PubMed  CAS  Google Scholar 

  43. 43.

    Schaller GE, Shiu SH, Armitage JP (2011) Two-component systems and their co-option for eukaryotic signal transduction. Curr Biol 21:R320–R330

    PubMed  CAS  Google Scholar 

  44. 44.

    Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–10123

    PubMed  CAS  Google Scholar 

  45. 45.

    Desikan R, Horák J, Chaban C, Mira-Rodado V, Witthöft J, Elgass K, Grefen C, Cheung MK, Meixner AJ, Hooley R, Neill SJ, Hancock JT, Harter K (2008) The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLoS One 3(6):e2491

    PubMed  Google Scholar 

  46. 46.

    Desikan R, Hancock JT, Bright J, Harrison J, Weir I, Hooley R, Neill SJ (2005) A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol 137:831–834

    PubMed  CAS  Google Scholar 

  47. 47.

    Wang W, Hall AE, O’Malley R, Bleecker AB (2003) Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc Natl Acad Sci USA 100:352–357

    PubMed  CAS  Google Scholar 

  48. 48.

    Singh KK (2000) The Saccharomyces cerevisiae Sln1p–Ssk1p two-component system mediates response to oxidative stress and in an oxidant-specific fashion. Free Radic Biol Med 29:1043–1050

    PubMed  CAS  Google Scholar 

  49. 49.

    Buck V, Quinn J, Soto Pino T, Martin H, Saldanha J, Makino K, Morgan BA, Millar JB (2001) Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol Biol Cell 12:407–419

    PubMed  CAS  Google Scholar 

  50. 50.

    Day AM, Veal EA (2010) Hydrogen peroxide-sensitive cysteines in the Sty1 MAPK regulate the transcriptional response to oxidative stress. J Biol Chem 285:7505–7516

    PubMed  CAS  Google Scholar 

  51. 51.

    Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoumskaya M, Suzuki I, Hayashi H, Murata N (2007) Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803. Plant J 49:313–324

    PubMed  CAS  Google Scholar 

  52. 52.

    Matsubara M, Mizuno T (2000) The SixA phospho-histidine phosphatase modulates the ArcB phosphorelay signal transduction in Escherichia coli. FEBS Lett 470:118–124

    PubMed  CAS  Google Scholar 

  53. 53.

    Wang M, Jiang YY, Kim KM, Qu G, Ji HF, Mittenthal JE, Zhang HY, Caetano-Anollés G (2011) A universal molecular clock of protein folds and its power in tracing the early history of aerobic metabolism and planet oxygenation. Mol Biol Evol 1:567–582

    Google Scholar 

  54. 54.

    Oh JI, Kaplan S (2000) Redox signaling: globalization of gene expression. EMBO J 19:4237–4247

    PubMed  CAS  Google Scholar 

  55. 55.

    Balázsi G, van Oudenaarden A, Collins JJ (2011) Cellular decision making and biological noise: from microbes to mammals. Cell 144:910–925

    PubMed  Google Scholar 

  56. 56.

    Dawkins R (2006) The selfish gene (30th anniversary edition). Oxford University Press, New York

    Google Scholar 

  57. 57.

    Kushwah S, Jones AM, Laxmi A (2011) Cytokinin interplay with ethylene, auxin, and glucose signaling controls Arabidopsis seedling root directional growth. Plant Physiol 156:1851–1866

    PubMed  CAS  Google Scholar 

  58. 58.

    Tiwari A, Balázsi G, Gennaro ML, Igoshin OA (2010) The interplay of multiple feedback loops with post-translational kinetics results in bistability of mycobacterial stress response. Phys Biol 7:036005

    PubMed  Google Scholar 

  59. 59.

    Ray JC, Igoshin OA (2010) Adaptable functionality of transcriptional feedback in bacterial two-component systems. PLoS Comput Biol 6:e1000676

    PubMed  Google Scholar 

  60. 60.

    Vandenbroucke K, Robbens S, Vandepoele K, Inzé D, Van de Peer Y, Van Breusegem F (2008) Hydrogen peroxide-induced gene expression across kingdoms: a comparative analysis. Mol Biol Evol 25:507–516

    PubMed  CAS  Google Scholar 

  61. 61.

    Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500

    PubMed  CAS  Google Scholar 

  62. 62.

    Rao GN, Berk BC (1992) Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res 70:593–599

    PubMed  CAS  Google Scholar 

  63. 63.

    Mesquita FS, Dyer SN, Heinrich DA, Bulun SE, Marsh EE, Nowak RA (2010) Reactive oxygen species mediate mitogenic growth factor signaling pathways in human leiomyoma smooth muscle cells. Biol Reprod 82:341–351

    PubMed  CAS  Google Scholar 

  64. 64.

    Arana L, Gangoiti P, Ouro A, Rivera IG, Ordoñez M, Trueba M, Lankalapalli RS, Bittman R, Gomez-Muñoz A (2012) Generation of reactive oxygen species (ROS) is a key factor for stimulation of macrophage proliferation by ceramide 1-phosphate. Exp Cell Res 318:350–360

    PubMed  CAS  Google Scholar 

  65. 65.

    Iruthayanathan M, O’Leary B, Paul G, Dillon JS (2011) Hydrogen peroxide signaling mediates DHEA-induced vascular endothelial cell proliferation. Steroids 76:1483–1490

    PubMed  CAS  Google Scholar 

  66. 66.

    Brown MR, Miller FJ Jr, Li WG, Ellingson AN, Mozena JD, Chatterjee P, Engelhardt JF, Zwacka RM, Oberley LW, Fang X, Spector AA, Weintraub NL (1999) Overexpression of human catalase inhibits proliferation and promotes apoptosis in vascular smooth muscle cells. Circ Res 85(6):524–533

    PubMed  CAS  Google Scholar 

  67. 67.

    Shi M, Yang H, Motley ED, Guo Z (2004) Overexpression of Cu/Zn-superoxide dismutase and/or catalase in mice inhibits aorta smooth muscle cell proliferation. Am J Hypertens 17:450–456

    PubMed  CAS  Google Scholar 

  68. 68.

    Davies KJ (1999) The broad spectrum of responses to oxidants in proliferating cells: a new paradigm for oxidative stress. IUBMB Life 48:41–47

    PubMed  CAS  Google Scholar 

  69. 69.

    Burch PM, Heintz NH (2005) Redox regulation of cell-cycle re-entry: cyclin D1 as a primary target for the mitogenic effects of reactive oxygen and nitrogen species. Antioxid Redox Signal 7:741–751

    PubMed  CAS  Google Scholar 

  70. 70.

    Menon SG, Goswami PC (2007) A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26:1101–1109

    PubMed  CAS  Google Scholar 

  71. 71.

    Sarsour EH, Kumar MG, Chaudhuri L, Kalen AL, Goswami PC (2009) Redox control of the cell cycle in health and disease. Antioxid Redox Signal 11:2985–3011

    PubMed  CAS  Google Scholar 

  72. 72.

    Beveridge CA, Mathesius U, Rose RJ, Gresshoff PM (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51

    PubMed  CAS  Google Scholar 

  73. 73.

    Chen Z, Odstrcil EA, Tu BP, McKnight SL (2007) Restriction of DNA replication to the reductive phase of the metabolic cycle protects genome integrity. Science 316:1916–1919

    PubMed  CAS  Google Scholar 

  74. 74.

    Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

    PubMed  CAS  Google Scholar 

  75. 75.

    Dunand C, Crèvecoeur M, Penel C (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol 174:332–341

    PubMed  CAS  Google Scholar 

  76. 76.

    Owusu-Ansah E, Banerjee U (2009) Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461:537–541

    PubMed  CAS  Google Scholar 

  77. 77.

    Peraza L, Hansberg W (2002) Neurospora crassa catalases, singlet oxygen and cell differentiation. Biol Chem 383:569–575

    PubMed  CAS  Google Scholar 

  78. 78.

    Toledo I, Rangel P, Hansberg W (1995) Redox imbalance at the start of each morphogenetic step of Neurospora crassa conidiation. Arch Biochem Biophys 319:519–524

    PubMed  CAS  Google Scholar 

  79. 79.

    Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    PubMed  Google Scholar 

  80. 80.

    Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168

    PubMed  CAS  Google Scholar 

  81. 81.

    Hazan R, Sat B, Engelberg-Kulka H (2004) Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J Bacteriol 186:3663–3669

    PubMed  CAS  Google Scholar 

  82. 82.

    Lewis K (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64:503–514

    PubMed  CAS  Google Scholar 

  83. 83.

    van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761

    PubMed  Google Scholar 

  84. 84.

    Meyer Y, Belin C, Delorme-Hinoux V, Recihheld JP, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, cross talks and functional significance. Antioxid Redox Signal. doi:10.1089/ars.2011.4327

    PubMed  Google Scholar 

  85. 85.

    Fernandes AP, Holmgren A (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6:63–74

    PubMed  CAS  Google Scholar 

  86. 86.

    Zaffagnini M, Bedhomme M, Lemaire SD, Trost P (2012) The emerging roles of protein glutathionylation in chloroplasts. Plant Sci 186:86–96

    Google Scholar 

  87. 87.

    Iwema T, Picciocchi A, Traore DA, Ferrer JL, Chauvat F, Jacquamet L (2009) Structural basis for delivery of the intact [Fe2–S2] cluster by monothiol glutaredoxin. Biochemistry 48:6041–6043

    PubMed  CAS  Google Scholar 

  88. 88.

    Li H, Mapolelo DT, Dingra NN, Naik SG, Lees NS, Hoffman BM, Riggs-Gelasco PJ, Huynh BH, Johnson MK, Outten CE (2009) The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe–2S] cluster with cysteinyl and histidyl ligation. Biochemistry 48:9569–9581

    PubMed  CAS  Google Scholar 

  89. 89.

    Faulkner MJ, Veeravalli K, Gon S, Georgiou G, Beckwith J (2008) Functional plasticity of a peroxidase allows evolution of diverse disulfide-reducing pathways. Proc Natl Acad Sci USA 105:6735–6740

    PubMed  CAS  Google Scholar 

  90. 90.

    Boal AK, Cotruvo JA Jr, Stubbe J, Rosenzweig AC (2010) Structural basis for activation of class Ib ribonucleotide reductase. Science 329:1526–1530

    PubMed  CAS  Google Scholar 

  91. 91.

    Chartron J, Shiau C, Stout CD, Carroll KS (2007) 3′-Phosphoadenosine-5′-phosphosulfate reductase in complex with thioredoxin: a structural snapshot in the catalytic cycle. Biochemistry 46:3942–3951

    PubMed  CAS  Google Scholar 

  92. 92.

    Moskovitz J, Oien DB (2010) Protein carbonyl and the methionine sulfoxide reductase system. Antioxid Redox Signal 12:405–415

    PubMed  CAS  Google Scholar 

  93. 93.

    Laugier E, Tarrago L, Vieira Dos Santos C, Eymery F, Havaux M, Rey P (2010) Arabidopsis thaliana plastidial methionine sulfoxide reductases B, MSRBs, account for most leaf peptide MSR activity and are essential for growth under environmental constraints through a role in the preservation of photosystem antennae. Plant J 61:271–282

    PubMed  CAS  Google Scholar 

  94. 94.

    Kim SO, Merchant K, Nudelman R, Beyer WF Jr, Keng T, DeAngelo J, Hausladen A, Stamler JS (2002) OxyR: a molecular code for redox-related signaling. Cell 109:383–396

    PubMed  CAS  Google Scholar 

  95. 95.

    Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159

    PubMed  CAS  Google Scholar 

  96. 96.

    Matsui M, Oshima M, Oshima H, Takaku K, Maruyama T, Yodoi J, Taketo MM (1996) Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev Biol 178:179–185

    PubMed  CAS  Google Scholar 

  97. 97.

    Neumann CA, Cao J (2009) Manevich Y (2009) Peroxiredoxin 1 and its role in cell signaling. Cell Cycle 8:4072–4078

    PubMed  CAS  Google Scholar 

  98. 98.

    Ando K, Hirao S, Kabe Y, Ogura Y, Sato I, Yamaguchi Y, Wada T, Handa H (2008) A new APE1/Ref-1-dependent pathway leading to reduction of NF-kappaB and AP-1, and activation of their DNA-binding activity. Nucleic Acids Res 36:4327–4336

    PubMed  CAS  Google Scholar 

  99. 99.

    Dai S, Schwendtmayer C, Schürmann P, Ramaswamy S, Eklund H (2000) Redox signaling in chloroplasts: cleavage of disulfides by an iron–sulfur cluster. Science 287:655–658

    PubMed  CAS  Google Scholar 

  100. 100.

    Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19:1851–1865

    PubMed  CAS  Google Scholar 

  101. 101.

    Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D, May MJ, Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110

    PubMed  CAS  Google Scholar 

  102. 102.

    Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardó FV, Pellny TK, Verrier PJ, Foyer CH (2010) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 64:825–838

    PubMed  CAS  Google Scholar 

  103. 103.

    Markovic J, Borrás C, Ortega A, Sastre J, Viña J, Pallardó FV (2007) Glutathione is recruited into the nucleus in early phases of cell proliferation. J Biol Chem 282:20416–22024

    PubMed  CAS  Google Scholar 

  104. 104.

    Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106:3615–3620

    PubMed  CAS  Google Scholar 

  105. 105.

    Kruger NJ, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 6:236–246

    PubMed  CAS  Google Scholar 

  106. 106.

    Wenderoth I, Scheibe R, von Schaewen A (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J Biol Chem 272:26985–26990

    PubMed  CAS  Google Scholar 

  107. 107.

    Barajas-López Jde D, Serrato AJ, Cazalis R, Meyer Y, Chueca A, Reichheld JP, Sahrawy M (2011) Circadian regulation of chloroplastic f and m thioredoxins through control of the CCA1 transcription factor. J Exp Bot 62:2039–2051

    PubMed  Google Scholar 

  108. 108.

    McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    PubMed  CAS  Google Scholar 

  109. 109.

    Comelli RN, Gonzalez DH (2007) Conserved homeodomain cysteines confer redox sensitivity and influence the DNA binding properties of plant class III HD-Zip proteins. Arch Biochem Biophys 467:41–47

    PubMed  CAS  Google Scholar 

  110. 110.

    Williams JC, Sue C, Banting GS, Yang H, Glerum DM, Hendrickson WA, Schon EA (2005) Crystal structure of human SCO1: implications for redox signaling by a mitochondrial cytochrome c oxidase “assembly” protein. J Biol Chem 280:15202–15211

    PubMed  CAS  Google Scholar 

  111. 111.

    Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes (corrected) of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956

    PubMed  CAS  Google Scholar 

  112. 112.

    Rouhier N, Gelhaye E, Jacquot JP (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266–1277

    PubMed  CAS  Google Scholar 

  113. 113.

    Xing S, Rosso MG, Zachgo S (2005) ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development 132:1555–1565

    PubMed  CAS  Google Scholar 

  114. 114.

    Reichheld JH, Riondet C, Delorme V, Vignols F, Meyer Y (2010) Thioredoxins and glutaredoxins in development. Plant Science 178:420–423

    CAS  Google Scholar 

  115. 115.

    Xing S, Zachgo S (2008) ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J 53:790–801

    PubMed  CAS  Google Scholar 

  116. 116.

    Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S (2009) Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana. Plant Cell 21:429–441

    PubMed  CAS  Google Scholar 

  117. 117.

    Chuang CF, Running MP, Williams RW, Meyerowitz EM (1999) The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana. Genes Dev 13:334–344

    PubMed  CAS  Google Scholar 

  118. 118.

    Maier AT, Stehling-Sun S, Wollmann H, Demar M, Hong RL, Haubeiss S, Weigel D, Lohmann JU (2009) Dual roles of the bZIP transcription factor PERIANTHIA in the control of floral architecture and homeotic gene expression. Development 136:1613–1620

    PubMed  CAS  Google Scholar 

  119. 119.

    Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR (2010) Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol 154:1492–1504

    PubMed  CAS  Google Scholar 

  120. 120.

    Riondet C, Desouris JP, Montoya JG, Chartier Y, Meyer Y, Reichheld JP (2012) A dicotyledon-specific glutaredoxin GRXC1 family with dimer-dependent redox regulation is functionally redundant with GRXC2. Plant Cell Environ 35:360–373

    PubMed  CAS  Google Scholar 

  121. 121.

    Cheng NH, Liu JZ, Liu X, Wu Q, Thompson SM, Lin J, Chang J, Whitham SA, Park S, Cohen JD, Hirschi KD (2011) Arabidopsis monothiol glutaredoxin, AtGRXS17, is critical for temperature-dependent postembryonic growth and development via modulating auxin response. J Biol Chem 286:20398–20406

    PubMed  CAS  Google Scholar 

  122. 122.

    Laporte D, Olate E, Salinas P, Salazar M, Jordana X, Holuigue L (2012) Glutaredoxin GRXS13 plays a key role in protection against photooxidative stress in Arabidopsis. J Exp Bot 63:503–515

    PubMed  CAS  Google Scholar 

  123. 123.

    Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468

    PubMed  CAS  Google Scholar 

  124. 124.

    Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159

    PubMed  CAS  Google Scholar 

  125. 125.

    Fourquet S, Huang ME, D’Autreaux B, Toledano MB (2008) The dual functions of thiol-based peroxidases in H2O2 scavenging and signaling. Antioxid Redox Signal 10:1565–1576

    PubMed  CAS  Google Scholar 

  126. 126.

    D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813–824

    PubMed  Google Scholar 

  127. 127.

    Jara M, Vivancos AP, Calvo IA, Moldón A, Sansó M, Hidalgo E (2007) The peroxiredoxin Tpx1 is essential as a H2O2 scavenger during aerobic growth in fission yeast. Mol Biol Cell 18:2288–2295

    PubMed  CAS  Google Scholar 

  128. 128.

    Vivancos AP, Castillo EA, Biteau B, Nicot C, Ayté J, Toledano MB, Hidalgo E (2005) A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci USA 102:8875–8880

    PubMed  CAS  Google Scholar 

  129. 129.

    Veal EA, Findlay VJ, Day AM, Bozonet SM, Evans JM, Quinn J, Morgan BA (2004) A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol Cell 15:129–139

    PubMed  CAS  Google Scholar 

  130. 130.

    Fomenko DE, Koc A, Agisheva N, Jacobsen M, Kaya A, Malinouski M, Rutherford JC, Siu KL, Jin DY, Winge DR, Gladyshev VN (2011) Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proc Natl Acad Sci USA 108:2729–2734

    PubMed  CAS  Google Scholar 

  131. 131.

    Uhlich GA (2009) KatP contributes to OxyR-regulated hydrogen peroxide resistance in Escherichia coli serotype O157: H7. Microbiology 155:3589–3598

    PubMed  CAS  Google Scholar 

  132. 132.

    Kang SW, Chae HZ, Seo MS, Kim K, Baines IC, Rhee SG (1998) Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J Biol Chem 273:6297–6302

    PubMed  CAS  Google Scholar 

  133. 133.

    Brigelius-Flohé R, Flohé L (2011) Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 15:2335–2338

    PubMed  Google Scholar 

  134. 134.

    Haslekås 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 53:313–326

    PubMed  Google Scholar 

  135. 135.

    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 19:4120–4130

    PubMed  CAS  Google Scholar 

  136. 136.

    Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180

    PubMed  CAS  Google Scholar 

  137. 137.

    Baier M, Noctor G, Foyer CH, Dietz KJ (2000) Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol 124:823–832

    PubMed  CAS  Google Scholar 

  138. 138.

    Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schöttler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A, Weis E, Miginiac-Maslow M, Dietz KJ (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981

    PubMed  CAS  Google Scholar 

  139. 139.

    Chang CC, Slesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150:670–683

    PubMed  CAS  Google Scholar 

  140. 140.

    Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766

    PubMed  CAS  Google Scholar 

  141. 141.

    Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132:603–614

    PubMed  CAS  Google Scholar 

  142. 142.

    Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403

    PubMed  CAS  Google Scholar 

  143. 143.

    Kawahara T, Quinn MT, Lambeth JD (2007) Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol Biol 6(7):109

    Google Scholar 

  144. 144.

    Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    PubMed  CAS  Google Scholar 

  145. 145.

    Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751

    PubMed  Google Scholar 

  146. 146.

    Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699

    PubMed  CAS  Google Scholar 

  147. 147.

    Chen K, Craige SE, Keaney JF Jr (2009) Downstream targets and intracellular compartmentalization in Nox signaling. Antioxid Redox Signal 11:2467–2480

    PubMed  CAS  Google Scholar 

  148. 148.

    Zamocky M, Furtmüller PG, Obinger C (2011) Evolution of catalases from bacteria to humans. Antioxid Redox Signal 10:1527–1548

    Google Scholar 

  149. 149.

    Miller AF (2012) Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 586:585–595

    PubMed  CAS  Google Scholar 

  150. 150.

    Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O’Neill JS, Reddy AB (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–464

    PubMed  CAS  Google Scholar 

  151. 151.

    Goyal A, Tolbert NE (1989) Variations in the alternative oxidase in Chlamydomonas grown in air or high CO2. Plant Physiol 89:958–962

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Jos H. M. Schippers or Bernd Mueller-Roeber.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schippers, J.H.M., Nguyen, H.M., Lu, D. et al. ROS homeostasis during development: an evolutionary conserved strategy. Cell. Mol. Life Sci. 69, 3245–3257 (2012). https://doi.org/10.1007/s00018-012-1092-4

Download citation

Keywords

  • Evolution
  • Reactive oxygen species
  • Development