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ROS: Central Component of Signaling Network in Plant Cell

  • Soumen Bhattacharjee
Chapter

Abstract

Plants often deliberately generate and exploit reactive oxygen species (ROS) or its secondary breakdown products for a number of processes ranging from cell signaling to gene expression. The cellular language associated with ROS signaling network involves a close coordination of four interacting phenomenons, ranging from ROS sensing, signaling, differential expression of redox-sensitive genes, and influencing stress and developmental responses of the plant. The role of ROS as “second messenger” modulating the activities of specific transcription factors or functional proteins is well elucidated. Apart from its bona fide role in the signaling cascades, ROS often complements, synergizes, and antagonizes several growth regulatory circuits through cross talking with other signaling molecules. In this perspective, understanding the mechanism of ROS sensing associated with subsequent signaling cascades in plant cell is not only fundamental but also of immense practical significance, since this knowledge may contribute significantly in agricultural productivity by better management of environmental and oxidative stress. The position of these prooxidants under environmental stress demonstrated that it is essential for the perception and communication of environmental stimuli and associated developmental processes. The retrograde signaling induced by ROS are extremely significant in maintaining cellular redox homeostasis and controlling systemic signaling cascades associated with stress acclamatory responses. Apart from the direct role of ROS in cell signaling, some of the products of oxidative stress, particularly reactive lipid species (RLS), also represent “biological signals,” which do not need preceding activation of genes. In the present chapter, an effort has been made to discuss the mechanism of ROS sensing in the elaborate signaling network of plant cell. The present chapter also explores both the mechanisms of signaling cascade of ROS in plant acclamatory defense processes, controlled cell death, and development. The role of redox-sensitive proteins in ROS signaling, its subsequent regulation of Ca2+ homeostasis, and MAPK cascades is also discussed. An additional effort has been made to understand the mechanism of H2O2-regulated gene expression in plant cell.

Keywords

ROS Signal transduction Redox sensing Redox-regulated gene expression Redox-sensitive proteins Lipid peroxidation products Oxylipin 

References

  1. Agrawal GK, Iwahashi H, Rakwal R (2003) Small GTPase ‘Rop’: molecular switch for plant defense responses. FEBS Lett 546:173–180CrossRefGoogle Scholar
  2. Ahn SG, Thiele DJ (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17:516–528CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen JF (1993) Redox control of transcription: sensors, response regulators, activators and suppressors. FEBS Lett 332:203–207CrossRefGoogle Scholar
  4. Allen RG, Tresini M (2002) Oxidative stress and gene regulation. Free Radic Biol Med 28:463–499CrossRefGoogle Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  6. Arrigo AP (1999) Gene expression and the thiol redox state. Free Radic Biol Med 27:936–945CrossRefGoogle Scholar
  7. Asai A, Qui J, Narita Y (1999) High level calcineurin activity predisposes neuronal cells to apoptosis. J Biol Chem 274:34450–34458CrossRefGoogle Scholar
  8. Balazadeh S, Wu A, Mueller-Roeber B (2010a) Salt-triggered expression of the ANAC092-dependent senescence regulon in Arabidopsis thaliana. Plant Signal Behav 5:733–735CrossRefPubMedPubMedCentralGoogle Scholar
  9. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Kohler B, Mueller-Roeber B (2010b) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62:250–264CrossRefGoogle Scholar
  10. Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor MI, Xue GP, Mueller- Roeber B (2011) ORS1, an H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4:346–360CrossRefPubMedPubMedCentralGoogle Scholar
  11. Benabdellah K, Ruiz-Lozano JM, Aroca R (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol Biol 70:647–661CrossRefGoogle Scholar
  12. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:113–1121Google Scholar
  13. Bhattacharjee S (2008) Calcium-dependent signaling pathway in heat-induced oxidative injury in Amaranthus lividus. Biol Plant 52:1137–1140CrossRefGoogle Scholar
  14. Bhattacharjee S (2010) Sites of generation and physicochemical basis of formation of reactive oxygen species in plant cell. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. Science Pubication. CRC Press, Boca Raton, pp 01–30Google Scholar
  15. Bhattacharjee S (2012) An inductive pulse of hydrogen peroxide pretreatment restores redox- homeostasis andmitigates oxidative membrane damage under extremes of temperature in two rice cultivars (Oryza sativa L., Cultivars Ratna and SR 26B). Plant Growth Regul 68:395–410CrossRefGoogle Scholar
  16. Bienert GP, Møller ALB, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bolwell GP, Bnti VS, Davis DR, Zinmorlin A (1995) The origin of oxidative burst in plants. Free Radic Res 23:517–532CrossRefGoogle Scholar
  18. Buchanon BB (1980) Role of light in regulation of chloroplastic enzymes. Annu Rev Plant Physiol 31:341–374CrossRefGoogle Scholar
  19. Chen Z, Silva H, Klessig DF (1993a) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886CrossRefGoogle Scholar
  20. Chen Z, Silva H, Klessig DF (1993b) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1886–1891CrossRefGoogle Scholar
  21. Chen W, Chao G, Singh KB (1996) The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J 10:955–963CrossRefGoogle Scholar
  22. Chowdhury FK, Rivero FM, Blumwald E, Mittler R (2016) Reactive oxygen species, abiotic stress and stress combination. Plant J.  https://doi.org/10.1111/tpj.13299
  23. Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268CrossRefGoogle Scholar
  24. Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H Jr, Van Montagu M, Inzé D, Van Camp W (1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic plants. Proc Natl Acad Sci U S A 95:5818–5823Google Scholar
  25. Cunninghum KW, Fink GK (1996) Calcineurin-dependent inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+-ATPases in Saccharomyces cerevisiae. Mol Cell Biol 16:2226–2237CrossRefGoogle Scholar
  26. Daniel V (1993) Glutathione S-transferases: gene structure and regulation of expression. Crit Rev Biochem Mol Biol 28:173–207CrossRefGoogle Scholar
  27. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281CrossRefPubMedPubMedCentralGoogle Scholar
  28. Demple B (1991) Regulation of bacterial oxidative stress genes. Annu Rev Gen 25:315–337CrossRefGoogle Scholar
  29. Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZip DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726 734CrossRefGoogle Scholar
  30. Dubbs JM, Mongkolsuk S (2012) Peroxide-sensing transcriptional regulators in bacteria. J Bacteriol 194:5495–5503CrossRefPubMedPubMedCentralGoogle Scholar
  31. Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem J 414:53–61CrossRefPubMedPubMedCentralGoogle Scholar
  32. Eggler AL, Liu G, Pezzuto JM, van Breemen RB, Mesecar AD (2005) Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc Natl Acad Sci U S A 102:10070–10075CrossRefPubMedPubMedCentralGoogle Scholar
  33. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signalling. Curr Opin Plant Biol 10:366–371CrossRefPubMedPubMedCentralGoogle Scholar
  34. Fernandes L, Rodrigues-Pousada C, Struhl K (1997) Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol Cell Biol 17:6982–6993CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ferrer-Sueta G, Manta B, Botti H, Radi R, Trujillo M, Denicola A (2011) Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem Res Toxicol 24:434–450CrossRefGoogle Scholar
  36. 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 422:442–446CrossRefPubMedPubMedCentralGoogle Scholar
  37. Friling RS, Bergelson S, Daniel V (1992) Two adjacent AP-1-like binding sites from the electrophile-responsive element of the murine glutathione S-transferase Ya subunit gene. Proc Natl Acad Sci U S A 89:668–673CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signalling in Arabidopsis. Plant Physiol 141:436–445CrossRefPubMedPubMedCentralGoogle Scholar
  39. Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 8:17–20CrossRefGoogle Scholar
  40. 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. Int Union Biochem Mol Biol Life 57:181–188CrossRefGoogle Scholar
  41. Ghesquière B, Jonckheere V, Colaert N, Van Durme J, Timmerman E, Goethals M, Schymkowitz J, Rousseau F, Vandekerckhove J, Gevaert K (2011) Redox proteomics of protein-bound methionine oxidation. Mol Cell Proteomics 10:M110.006866CrossRefPubMedPubMedCentralGoogle Scholar
  42. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedPubMedCentralGoogle Scholar
  43. Godon C, Lagniel G, Lee J, Buhler JM, Kieffer S, Perrot M, Boucherie H, Toledano MB, Labarre J (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273:224–280CrossRefGoogle Scholar
  44. Gong M, Li YJ, Chen SZ (1998) ABA induced thermotolerance in maize seedlings is mediated by calcium and associated antioxidant systems. J Plant Physiol 153:488–497CrossRefGoogle Scholar
  45. Gosti F, Beandoin N, Serizet C, Webb AAR, Vertanian N, Giraudat T (1993) AB11 protein phosphatase 2C is a negative regulator of ABA signaling. Plant Cell 11:1897–1903CrossRefGoogle Scholar
  46. Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:441–450CrossRefPubMedPubMedCentralGoogle Scholar
  47. Grosch W (1982) Lipid degradation products and flavor. In: Morton ID, Mac Leod AJ (eds) Food flavours. Elsevier, Amsterdam, pp 325–398Google Scholar
  48. Guan ZM, Zhao J, Scandalios JG (2000) Cis-elements and trans-factors that regulate expression of maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–98Google Scholar
  49. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322CrossRefPubMedPubMedCentralGoogle Scholar
  50. Helmann JD, Wu MF, Gaballa A, Kobel PA, Morshedi MM, Fawcett P, Paddon C (2003) The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J Bacteriol 185:243–253CrossRefPubMedPubMedCentralGoogle Scholar
  51. Higden A, Olver AR, Jyob J, Lender A, Darlayusmer VM (2012) Cell signalling by reactive lipid species: new concept and molecular mechanism. Biochem J 442:453–464CrossRefGoogle Scholar
  52. Ivenish G, Tillberg EJ (1995) Stress-induced ethylene biosynthesis in pine needles: a search for putative ACC- independent pathway. Plant Physiol 145:308–317CrossRefGoogle Scholar
  53. Karimpour S, Lou J, Lin LL, Rene LM, Langunas L, Ma X, Karra S, Bradbarey CM, Markovina S, Goswami PC et al (2002) Thioredoxin reductase regulates AP-1 activity as well as thioredoxin nuclear localization via active cysteines in response to ionizing radiation. Oncogene 21:6317–6327CrossRefPubMedPubMedCentralGoogle Scholar
  54. Krebs J (1998) The role of calcium in apoptosis. Biometals 11:375–382CrossRefGoogle Scholar
  55. 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 109:383–396CrossRefGoogle Scholar
  56. Kovalchuk I (2010) Multiple roles of radicals in plants. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. Science Pubication. CRC Press, Boca Raton, pp 31–44CrossRefGoogle Scholar
  57. Kurepa J, Herooart D, Van Motague M, Inze D (1997) Differential expression of cu, Zn and Fe- superoxidedismutase genes of tobacco during development, oxidative stress and hormonal treatments. Plant Cell Physiol 38:463–473CrossRefPubMedPubMedCentralGoogle Scholar
  58. Lachaud C, Da Silva D, Amelot N, Beziat C, Briere C, Cotelle V, Graziana A, Grat S, Mazars C, Thuleau P (2011) Dihydrosphingosine-induced programmed cell death in tobacco BY-2 cells is independent of H2O2 production. Mol Plant 4:310–318CrossRefGoogle Scholar
  59. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC, Ahn WS, Yu MH, Storz G, Ryu SE (2004) Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11:1179–1185CrossRefGoogle Scholar
  61. Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1679CrossRefPubMedPubMedCentralGoogle Scholar
  62. Li T, Li H, Zhang YX, Liu JY (2011) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833CrossRefPubMedPubMedCentralGoogle Scholar
  63. Locato V, Pinto de MC, Paradiso A, Gara de L (2010) Reactive oxygen species and ascorbate – glutathione interplay in signaling and stress responses. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. Science Pubication. CRC Press, Boca Raton, pp 45–64CrossRefGoogle Scholar
  64. Lynch DV, Thompson JE (1984) Lipoxygenase mediated production of superoxide anion in senescing plant tissue. FEBS Lett 173:251–254CrossRefGoogle Scholar
  65. Mahalingam R, Fedoroff N (2003) Stress response, cell death and signaling. Physiol Plant 119:56–68CrossRefGoogle Scholar
  66. Marinho HS, Real C, Cyrne L, Soares H, Antunes F (2014) Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol 2:535–562CrossRefPubMedPubMedCentralGoogle Scholar
  67. Maxwell DP, Wang Y, McIntosh L (1999) Alternative oxidase lowers mitochondrial ROS production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276CrossRefPubMedPubMedCentralGoogle Scholar
  68. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867CrossRefPubMedPubMedCentralGoogle Scholar
  69. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signalling and abiotic stress. Physiol Plant 133:481–489CrossRefGoogle Scholar
  70. Miller G, Schlauch K, Tam R, Cortes D, Torres MA (2009) The plant NADPH oxidase RbohD mediates rapid, systemic signaling in response to diverse stimuli. Sci Signal 2(84):45–49CrossRefGoogle Scholar
  71. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467CrossRefPubMedPubMedCentralGoogle Scholar
  72. Miralto A, Barone G, Romano G, Poulet SA, Lanora A, Russo GL, Buttino I, Mazarella G, Laabir M, Cabrini M, Giacobbe MG (1999) The insidious effect of diatoms on copepod reproduction. Nature 402:173–176CrossRefGoogle Scholar
  73. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309CrossRefGoogle Scholar
  74. Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling. J Exp Bot 61:3577–3587CrossRefGoogle Scholar
  75. Mylona PV, Polidoros AN (2010) ROS regulation and antioxidant genes. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. Science Pubication. CRC Press, Boca Raton, pp 47–59Google Scholar
  76. Neill S, Desikan R, Clarke A, Harcock J (1999) H2O2 signaling in plant cells. In: Smallwood MF, Calvert CM, Bowles DJ (eds) Plant responses to environmental stresses. Bios Sci Pub, Oxford, pp 59–64Google Scholar
  77. Nishiyama A, Masutani H, Nakamura H, Nishinaka Y, Yodi J (2001) Redox regulation by thioredoxin and thioredoxin binding proteins. IUBMB Life 52:29–33CrossRefGoogle Scholar
  78. Noctor G, Foyer CH (1999) Ascorbate and glutathione:keeping active oxygen species under control. Annu Rev Plant Physiol Mol Biol 49:249–279CrossRefGoogle Scholar
  79. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734CrossRefGoogle Scholar
  80. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide-a central hub for information flow in plant cells. AoB Plants:pls014.  https://doi.org/10.1093/aobpla/pls014
  81. Polidoros AN, Scandalios JG (1999) Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol Plant 106:112–119CrossRefGoogle Scholar
  82. Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signalling in Arabidopsis. Plant Physiol 135:1471–1479CrossRefPubMedPubMedCentralGoogle Scholar
  83. Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 278:38921–38925CrossRefPubMedPubMedCentralGoogle Scholar
  84. Robson CA, Vanlerberghe GC (2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria –dependent and independent pathways of cell death. Plant Physiol 129:1908–1920CrossRefPubMedPubMedCentralGoogle Scholar
  85. Rouhier N, Lamaire SD, Jaqcquot JP (2009) The role of GSH in photosynthetic organisms: the emerging function of glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166CrossRefGoogle Scholar
  86. Sakamoto M (2008) Involvement of hyrogen peroxide in leaf abscission signaling revealed by analysis with an in vitro abscission system in Capsicum plants. Plant J 56:13–27CrossRefGoogle Scholar
  87. Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626CrossRefPubMedPubMedCentralGoogle Scholar
  88. Stephen DWS, Rivers SL, Jamieson DJ (1995) The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol Microbiol 16:415 423CrossRefGoogle Scholar
  89. Storz G, Tartaglia LA, Ames BN (1990) Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science (New York, NY) 248:189–194CrossRefGoogle Scholar
  90. Stremler KE, Staforrini DM, Prescott SM, Zimmerman GA, Mcintyre TM (1989) An oxidized derivative of phosphatidylcholine is a substrate for the platelet activating factor acetylhydrolase from human plasma. J Biol Chem 264:5331–5334PubMedGoogle Scholar
  91. Tonks NK (2005) Redox redux: revisiting PTPs and the control of cell signaling. Cell 121:667–670CrossRefPubMedPubMedCentralGoogle Scholar
  92. vanMontfort RL, Congreve M, Tisi D, Carr R, Jhoti H (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773–777CrossRefGoogle Scholar
  93. Varnova E, Langebartels C, Van Montague M, Inze D, Van Camp W (2000) Oxidative stress, heat shock and drought differentially affect expression of a tobacco protein phosphatase 2C. J Exp Bot 51:1763–1775CrossRefGoogle Scholar
  94. Varnova E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236CrossRefGoogle Scholar
  95. Veal EA, Day AM, Morgan BA (2007) Hydrogen peroxide sensing and signaling. Mol Cell 26:1–14CrossRefGoogle Scholar
  96. Wingate VPM, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–211CrossRefPubMedPubMedCentralGoogle Scholar
  97. Wu J, Shang Z, Wu J, Jiang X, Moschou PN, Sun W, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca(2+) -permeable channels and pollen tube growth. Plant J 63:1042–1053CrossRefGoogle Scholar
  98. Yamamoto A, Mizukami Y, Sakurai H (2005) Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J Biol Chem 280:11911–11919CrossRefGoogle Scholar
  99. Yamamoto A, Ueda J, Yamamoto N, Hashikawa N, Sakurai H (2007) Role of heat shock transcription factor in Saccharomyces cerevisiae oxidative stress response. Eukaryot Cell 6:1373–1379CrossRefPubMedPubMedCentralGoogle Scholar
  100. You J, Chan J (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant Sci.  https://doi.org/10.3389/fpls.2015.01092
  101. Zheng M, Aslund F, Storz G (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718–1721CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature India Private Limited 2019

Authors and Affiliations

  • Soumen Bhattacharjee
    • 1
  1. 1.Department of BotanyUGC Centre For Advanced Study, The University of BurdwanBurdwanIndia

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