Advertisement

ROS Signaling and Its Role in Plants

  • Mrinalini Manna
  • V. Mohan M. Achary
  • Malireddy K. ReddyEmail author
Chapter

Abstract

Reactive oxygen species (ROS) are the unavoidable byproducts of aerobic metabolism. They are the necessary evils for every living organism whose lives are dependent on atmospheric oxygen in one form or another. While excess level of ROS is toxic for the plants and causes oxidative stress, an optimum basal level of ROS is required to be maintained in the cells as it is indispensable for plant’s proper growth and development. Various latest studies have discovered that ROS signaling is essential for carrying out various biological activities such as cellular proliferation, differentiation, physiological cell death, cell-to-cell communication, stress acclimation, pathogen defense, and so on. Judicious manipulation of key regulators of ROS signaling can bring about improved adaptation of the plants to the recent climate changes happening across the globe.

Keywords

Adaptation Cell signaling Oxidative stress Reactive oxygen species homeostasis Stress response 

References

  1. Ahlfors R, Macioszek V, Rudd J, Brosché M, Schlichting R, Scheel D, Kangasjärvi J (2004) Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J Cell Mol Biol 40:512–522CrossRefGoogle Scholar
  2. Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559–1572PubMedPubMedCentralCrossRefGoogle Scholar
  3. Anbar AD (2008) Elements and evolution. Science 322:1481–1483PubMedCrossRefPubMedCentralGoogle Scholar
  4. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedCrossRefPubMedCentralGoogle Scholar
  5. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedPubMedCentralCrossRefGoogle Scholar
  6. Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt stress tolerance and blast disease resistance. Plant J 69:26–36PubMedCrossRefPubMedCentralGoogle Scholar
  7. Attacha S, Solbach D, Bela K, Moseler A, Wagner S, Schwarzländer M, Aller I, Müller SJ, Meyer AJ (2017) Glutathione peroxidase-like enzymes cover five distinct cell compartments and membrane surfaces in Arabidopsis thaliana. Plant Cell Environ 40:1281–1295PubMedCrossRefPubMedCentralGoogle Scholar
  8. Awad J, Stotz HU, Fekete A, Krischke M, Engert C, Havaux M, Berger S, Mueller MJ (2015) 2-cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water-water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions. Plant Physiol 167:1592–1603PubMedPubMedCentralCrossRefGoogle Scholar
  9. Barber J, Andersson B (1992) (1992) too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bienert GP, Møller ALB, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192PubMedCrossRefGoogle Scholar
  11. Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J, Rayapuram C, Idänheimo N, Hunter K, Kimura S, Merilo E, Vaattovaara A, Oracz K, Kaufholdt D, Pallon A, Anggoro DT, Glów D, Lowe J, Zhou J, Mohammadi O, Puukko T, Albert A, Lang H, Ernst D, Kollist H, Brosché M, Durner J, Borst JW, Collinge DB, Karpiński S, Lyngkjær MF, Robatzek S, Wrzaczek M, Kangasjärvi J (2015) Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLoS Genet 11:e1005373PubMedPubMedCentralCrossRefGoogle Scholar
  13. Boyd ES, Thomas KM, Dai Y, Boyd JM, Outten FW (2014) Interplay between oxygen and Fe–S cluster biogenesis: insights from the Suf pathway. Biochemistry 53:5834–5847PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brunkard JO, Runkel AM, Zambryski PC (2015) Chloroplasts extend stromules independently and in response to internal redox signals. Proc Natl Acad Sci U S A 112:10044–10049PubMedPubMedCentralCrossRefGoogle Scholar
  15. Burdiak P, Rusaczonek A, Witoń D, Głów D, Karpiński S (2015) Cysteine-rich receptorlike kinase CRK5 as a regulator of growth, development, and ultraviolet radiation responses in Arabidopsis thaliana. J Exp Bot 66:3325–3337PubMedPubMedCentralCrossRefGoogle Scholar
  16. Camp RGLO d, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332CrossRefGoogle Scholar
  17. Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, SanSegundo B (2014) Overexpression of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiol 165:688–704PubMedPubMedCentralCrossRefGoogle Scholar
  18. Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K, Modla S, Czymmek K, Dinesh-Kumar SP (2015) Chloroplast stromules function during innate immunity. Dev Cell 34:45–57PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chakraborty N, Tripathy BC (1992) 5-aminolevulinic acid induced photodynamic reactions in thylakoid membranes of cucumber (Cucumis sativus L.) cotyledons. J Plant Biochem Biotechnol 1:65–68CrossRefGoogle Scholar
  20. Chan KX, Mabbitt PD, Phua SY, Mueller JW, Nisar N, Gigolashvili T, Stroeher E, Grassl J, Arlt W, Estavillo GM, Jackson CJ, Pogson BJ (2016a) Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase. Proc Natl Acad Sci U S A 113:4567–4576CrossRefGoogle Scholar
  21. Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ (2016b) Learning the languages of the chloroplast: retrograde signaling and beyond. Annu Rev Plant Biol 67:25–53PubMedCrossRefPubMedCentralGoogle Scholar
  22. Chaouch S, Queval G, Vanderauwera S, Mhamdi A, Vandorpe M, Langlois- Meurinne M, Van Breusegem F, Saindrenan P, Noctor G (2010) Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiol 153:1692–1705PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cheng F, Blackburn K, Lin Y, Goshe MB, Williamson JD (2009) Absolute protein quantification by LC/MSE for global analysis of salicylic acid-induced plant protein secretion responses. J Proteome Res 8:82–93PubMedCrossRefGoogle Scholar
  24. Costa A, Drago I, Behera S, Zottini M, Pizzo P, Schroeder JI, Pozzan T, Schiavo FL (2010) H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2+- dependent scavenging system. Plant J Cell Mol Biol 62:760–772CrossRefGoogle Scholar
  25. Daloso DM, Müller K, Obata T, Florian A, Tohge T, Bottcher A, Riondet C, Bariat L, Carrari F, Nunes-Nesi A, Buchanan BB, Reichheld JP, Araújo WL, Fernie AR (2015) Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc Natl Acad Sci U S A 112:E1392–E1400PubMedPubMedCentralCrossRefGoogle Scholar
  26. De Clercq I, Vermeirssen V, Van Aken O, Vandepoele K, MMurcha MW, Law SR, Inzé A, Ng S, Ivanova A, Rombaut D, van de Cotte B, Jaspers P, Van de Peer Y, Kangasjärvi J, Whelan J, Van Breusegem F (2013) The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell 25:3472–3490PubMedPubMedCentralCrossRefGoogle Scholar
  27. de Souza A, Wang J-Z, Dehesh K (2017) Retrograde signals: integrators of interorganellar communication and orchestrators of plant development. Annu Rev Plant Biol 68:85–108PubMedCrossRefPubMedCentralGoogle Scholar
  28. Del Rio LA, Lopez-Huertas E (2016) ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol 57:1364–1376PubMedGoogle Scholar
  29. Delaunay A, Pflieger D, Barrault M-B, Vinh J, Toledano MB (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481PubMedCrossRefGoogle Scholar
  30. Deng X, Hu W, Wei S, Zhou S, Zhang F, Han J, Chen L, Li Y, Feng J, Fang B, Luo Q, Li S, Liu Y, Yang G, He G (2013) TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. PLoS One 8:e69881PubMedPubMedCentralCrossRefGoogle Scholar
  31. Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, Bennett M, Mansfield J, Zipfel C, Hamann T (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol 156:1364–1374PubMedPubMedCentralCrossRefGoogle Scholar
  32. Desikan R, Hancock JT, Ichimura K, Shinozaki K, Neill SJ (2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiol 126:1579–1587PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dong W, Wang M, Xu F, Quan T, Peng K, Xiao L, Xia G (2013) Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. PlantPhysiol 161:1217–1228Google Scholar
  35. Drazic A, MiuraH PJ, Le Y, Bach NC, Kriehuber T, Winter J (2013) Methionine oxidation activates a transcription factor in response to oxidative stress. Proc Natl Acad Sci U S A 110:9493–9498PubMedPubMedCentralCrossRefGoogle Scholar
  36. Drerup MM, Schlucking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569PubMedPubMedCentralCrossRefGoogle Scholar
  37. Droillard MJ, Boudsocq M, Barbier-Brygoo H, Laurière C (2004) Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 574:42–48PubMedCrossRefGoogle Scholar
  38. Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the beta-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1304–1318PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 110:8744–8749PubMedPubMedCentralCrossRefGoogle Scholar
  40. Erickson JL, Kantek M, Schattat MH (2017) Plastid-nucleus distance alters the behavior of stromules. Front Plant Sci 8:1135PubMedPubMedCentralCrossRefGoogle Scholar
  41. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012PubMedPubMedCentralCrossRefGoogle Scholar
  42. Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM (2017) Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signaling mechanism. Nat Commun 8:49PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fang Y, Liao K, Du H, Xu Y, Song H, Li X (2015) A stress- responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66:6803PubMedPubMedCentralCrossRefGoogle Scholar
  44. Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450PubMedCrossRefGoogle Scholar
  45. Fischer BB, Hideg E, Krieger-Liszkay A (2013) Production, detection, and signaling of singlet oxygen in photosynthetic organisms. Antioxid Redox Signal 18:2145–2162PubMedCrossRefGoogle Scholar
  46. Foote CS, Shook FC, Abakerli RB (1984) Characterization of singlet oxygen. Methods Enzymol 105:36–47PubMedCrossRefGoogle Scholar
  47. Foreman J, Demidchik V, Bothwell JHF, 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 422:442–446PubMedCrossRefGoogle Scholar
  48. Foyer CH, Noctor G (2016) Stress-triggered redox signalling: What’s in prospect? Plant Cell Environ 39:951–964PubMedCrossRefGoogle Scholar
  49. Foyer CH, Karpinska B, Krupinska K (2014) The functions of WHIRLY1 and REDOXRESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis. Philos Trans R Soc Lond Ser B Biol Sci 369:20130226CrossRefGoogle Scholar
  50. Frank HA, Young AJ, Britton G, Cogdell RJ (1999) The photochemistry of carotenoids. In: Advances in photosynthesis [and respiration], vol 8. Kluwer Academic Publishers. (now Springer, DordrechtGoogle Scholar
  51. Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates cross talk between submergence and drought tolerance in rice. Plant Cell 23:412–427PubMedCrossRefGoogle Scholar
  52. Garcia-Mata C, Wang J, Gajdanowicz P, Gonzalez W, Hills A, Donald N, Riedelsberger J, Amtmann A, Dreyer I, Blatt MR (2010) A minimal cysteine motif required to activate the SKOR K+ channel of Arabidopsis by the reactive oxygen species H2O2. J Biol Chem 285:29286–29294PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gawroński P, Witoń D, Vashutina K, Bederska M, Betliński B, Rusaczonek A, Karpiński S (2014) Mitogen-activated protein kinase 4 is a salicylic acid-independent regulator of growth but not of photosynthesis in Arabidopsis. Mol Plant 7:1151–1166PubMedCrossRefGoogle Scholar
  54. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147:595–610PubMedPubMedCentralCrossRefGoogle Scholar
  55. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 5th edn. Oxford university Press, OxfordGoogle Scholar
  56. Hanson MR, Sattarzadeh A (2013) Trafficking of proteins through plastid stromules. Plant Cell 25:2774–2782PubMedPubMedCentralCrossRefGoogle Scholar
  57. Havaux M, Dall’osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520PubMedPubMedCentralCrossRefGoogle Scholar
  58. He Y, Zhu ZJ (2008) Exogenous salicylic acid alleviates NaCl toxicity and increases antioxidative enzyme activity in Lycopersicon esculentum. Biol Plant 52:792–795CrossRefGoogle Scholar
  59. Hou X, Xie K, Yao J, Qi Z, Xiong L (2009) A homolog of human ski- interacting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci U S A 106:6410–6415PubMedPubMedCentralCrossRefGoogle Scholar
  60. Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133:170–181PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hu W, Huang C, Deng X, Zhou S, Chen L, Li Y, Wang C, Ma Z, Yuan Q, Wang Y, Cai R, Liang X, Yang G, He G (2013) TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. Plant Cell Environ 36:1449–1464PubMedCrossRefGoogle Scholar
  62. Hu DG, Ma QJ, Sun CH, Sun MH, You CX, Hao YJ (2015) Overexpression of MdSOS2L1, a CIPK protein kinase, increases the antioxidant metabolites to enhance salt tolerance in apple and tomato. Physiol Plant 156:201–214PubMedCrossRefGoogle Scholar
  63. Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817PubMedPubMedCentralCrossRefGoogle Scholar
  64. Huang S, Van Aken O, Schwarzl¨ander M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiol 171:1551–1559PubMedPubMedCentralCrossRefGoogle Scholar
  65. Huda KM, Banu MS, Garg B, Tula S, Tuteja R, Tuteja N (2013) OsACA6, a P-type IIB Ca2+ ATPase promotes salinity and drought stress tolerance in tobacco by ROS scavenging and enhancing the expression of stress-responsive genes. Plant J 76:997–1015PubMedCrossRefGoogle Scholar
  66. Irigoyen JJ, Perez de Juan J, Sanchez-Diaz M (1996) Drought enhances chilling tolerance in a chilling sensitive maize (Zea mays) variety. New Phytol 134:53–59CrossRefGoogle Scholar
  67. Jacques S, Ghesqui’ere 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
  68. Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, Cho D, Lee S, Giordo R, Sritubtim S, Leonhardt N, Ellis BE, Murata Y, Kwak JM (2009) MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci U S A 106:20520–20525PubMedPubMedCentralCrossRefGoogle Scholar
  69. Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161:1202–1216PubMedPubMedCentralCrossRefGoogle Scholar
  70. Jang SJ, Wi SJ, Choi YJ, An G, Park KY (2012) Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of Oryza sativa lysine decarboxylase-likeprotein1. MolCells 34:251–262Google Scholar
  71. Jung S, Lee HJ, Lee Y, Kang K, Kim YS, Grimm B, Back K (2008) Toxic tetrapyrrole accumulation in protoporphyrinogen IX oxidase-overexpressing transgenic rice plants. Plant Mol Biol 67:535–546PubMedCrossRefPubMedCentralGoogle Scholar
  72. Karpinski S, Szechynska-Hebda M, Wituszynska W, Burdiak P (2013) Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ 36:736–744PubMedCrossRefPubMedCentralGoogle Scholar
  73. Kaurilind E, Xu E, Brosché M (2015) A genetic framework for H2O2 induced cell death in Arabidopsis thaliana. BMC Genomics 16:837PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, Michikawa M, Kuchitsu K (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta 1823:398–405PubMedCrossRefGoogle Scholar
  76. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080PubMedPubMedCentralCrossRefGoogle Scholar
  77. Konopka-Postupolska D, Clark G, Goch G, Debski J, Floras K, Cantero A, Fijolek B, Roux S, Hennig J (2009) The role of annexin 1 in drought stress in Arabidopsis. Plant Physiol 150:1394–1410PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940–2945PubMedPubMedCentralCrossRefGoogle Scholar
  79. Krieger-Liszkay A, Trebst A (2006) Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction Centre. J Exp Bot 57:1677–1684PubMedCrossRefGoogle Scholar
  80. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedPubMedCentralCrossRefGoogle Scholar
  81. Laloi C, Havaux M (2015) Key players of singlet oxygen-induced cell death in plants. Front Plant Sci 6:39PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106PubMedCrossRefPubMedCentralGoogle Scholar
  83. Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:10270–10275PubMedPubMedCentralCrossRefGoogle Scholar
  84. Lee SH, Li CW, Koh KW, Chuang HY, Chen YR, Lin CS, Chan MT (2014) MSRB7reverses oxidation of GSTF2/3 to confer tolerance of Arabidopsis thaliana to oxidative stress. J Exp Bot 65:5049–5062PubMedPubMedCentralCrossRefGoogle Scholar
  85. Leister D (2017) Piecing the puzzle together: the central role of ROS and redox hubs in chloroplast retrograde signaling. Antioxid Redox Signal 30:1206–1219.Google Scholar
  86. Lermontova I, Grimm B (2006) Reduced activity of plastid protoporphyrinogen oxidase causes attenuated photodynamic damage during high-light compared to low-light exposure. Plant J 48:499–510PubMedCrossRefPubMedCentralGoogle Scholar
  87. Li Q, Yu B, Gao Y, Dai AH, Bai JG (2011) Cinnamic acid pretreatment mitigates chilling stress of cucumber leaves through altering antioxidant enzyme activity. J Plant Physiol 168:927–934PubMedCrossRefPubMedCentralGoogle Scholar
  88. Li CR, Liang DD, Li J, Duan YB, Li H, Yang YC, Qin RY, Li L, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress sinduction of rice ALTERNATIVE OXIDASE1 genes. Plant Cell Environ 36:775–788PubMedCrossRefPubMedCentralGoogle Scholar
  89. Lin F, Ding HD, Wang JX, Zhang H, Zhang AY, Zhang Y, Tan MP, Dong W, Jiang MY (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 60:3221–3238PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lin CC, Jih PJ, Lin HH, Lin JS, Chang LL, Shen YH, Jeng ST (2011) Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol Biol 77:235–249PubMedCrossRefGoogle Scholar
  91. Liu S, Wang M, Wei T, Meng C, Xia G (2014) A wheat SIMILAR TO RCD-ONE gene enhances seedling growth and abiotic stress resistance by modulating redox homeostasis and maintaining genomic integrity. Plant Cell 26:164–180PubMedPubMedCentralCrossRefGoogle Scholar
  92. Lu W, Chu X, Li Y, Wang C, Guo X (2013) Cotton GhMKK1 induces the tolerance of salt and drought stress, and mediates defence responses to pathogen infection in transgenic Nicotiana benthamiana. PLoS One 8:e68503PubMedPubMedCentralCrossRefGoogle Scholar
  93. Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317PubMedCrossRefGoogle Scholar
  94. Mateo A, Mühlenbock P, Rustérucci C, Chang CCC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830PubMedPubMedCentralCrossRefGoogle Scholar
  95. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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
  97. Meyer Y, Belin C, Delorme-Hinoux V, Reichheld J-P, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160PubMedCrossRefGoogle Scholar
  98. Miao Y, Lv D, Wang P, Wang X-C, 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 18:2749–2766PubMedPubMedCentralCrossRefGoogle Scholar
  99. Miller AF (2012) Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 586:585–595PubMedCrossRefGoogle Scholar
  100. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45PubMedPubMedCentralGoogle Scholar
  101. Mittler R (2016) ROS are good! Trends Plant Sci 22:11–19PubMedCrossRefGoogle Scholar
  102. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  103. 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 16:300–309PubMedCrossRefGoogle Scholar
  104. Mock HP, Grimm B (1997) Reduction of uroporphyrinogen decarboxylase by antisense RNA expression affects activities of other enzymes involved in tetrapyrrole biosynthesis and leads to light dependent necrosis. Plant Physiol 113:1101–1112PubMedPubMedCentralCrossRefGoogle Scholar
  105. Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci U S A 104:20996–21001PubMedPubMedCentralCrossRefGoogle Scholar
  106. Mozzo M, Dall’Osto L, Hienerwadel R, Bassi R, Croce R (2008) Photoprotection in the antenna complexes of photosystem II: role of individual xanthophylls in chlorophyll triplet quenching. J Biol Chem 283:6184–6192PubMedCrossRefGoogle Scholar
  107. Mühlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20:2339–2356PubMedPubMedCentralCrossRefGoogle Scholar
  108. Muhlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. Plant Cell 20:2339–2356PubMedPubMedCentralCrossRefGoogle Scholar
  109. Ng S, Ivanova A, Duncan O, Law SR, Van Aken O, De Clercq I, Wang Y, Carrie C, Xu L, Kmiec B, Walker H, Van Breusegem F, Whelan J, Giraud E (2013) A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25:3450–3471PubMedPubMedCentralCrossRefGoogle Scholar
  110. Ng S, De Clercq I, Van Aken O, Law SR, Ivanova A, Willems P, Giraud E, Van Breusegem F, Whelan J (2014) Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Mol Plant 7:1075–1093PubMedCrossRefPubMedCentralGoogle Scholar
  111. Nguyen HT, Cai S, Jiang G, Ye N, Chu Z, Xu X, Zhang J, Zhu G (2015) A key ABA catabolic gene, OsABA8ox3, is involved in drought stress resistance in rice. PLoS One 10:e0116646CrossRefGoogle Scholar
  112. Nie S, Yue H, Zhou J, Xing D (2015) Mitochondrial-derived reactive oxygen species play a vital role in the salicylic acid signaling pathway in Arabidopsis thaliana. PLoS One 10:e0119853PubMedPubMedCentralCrossRefGoogle Scholar
  113. Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. Plant J 61:1053–1066PubMedPubMedCentralCrossRefGoogle Scholar
  114. Ochsenbein C, Przybyla D, Danon A, Landgraf F, Göbel C, Imboden A, Feussner I, Apel K (2006) The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J Cell Mol Biol 47:445–456CrossRefGoogle Scholar
  115. Oda T, Hashimoto H, Kuwabara N, Hayashi K, Kojima C, Kawasaki T, Shimamoto K, Sato M, Shimizu T (2008) Crystallographic characterization of the N-terminal domain of a plant NADPH oxidase. Acta Crystallogr Sect F Struct Biol Cryst Commun 64:867–869PubMedPubMedCentralCrossRefGoogle Scholar
  116. Oda T, Hashimoto H, Kuwabara N, Akashi S, Hayashi K, Kojima C, Wong HL, Kawasaki T, Shimamoto K, Sato M, Shimizu T (2010) Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. J Biol Chem 285:1435–1445PubMedCrossRefGoogle Scholar
  117. Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892PubMedCrossRefPubMedCentralGoogle Scholar
  118. Ohad I, Keren N, Zer H, Gong H, Mor TS (1994) Light induced degradation of the photosystem II reaction center D1 protein in vivo: an integrative approach. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. BIOS Scientific Publishers, Oxford, pp 161–177Google Scholar
  119. Ortiz-Masia D, Perez-Amador MA, Carbonell J, Marcote MJ (2007) Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. FEBS Lett 581:1834–1840PubMedCrossRefPubMedCentralGoogle Scholar
  120. Pasqualini S, Piccioni C, Reale L, Ederli L, Della Torre G, Ferranti F (2003) Ozone-induced cell death in tobacco cultivar bel W3 plants. The role of programmed cell death in lesion formation. Plant Physiol 133:1122–1134PubMedPubMedCentralCrossRefGoogle Scholar
  121. Pérez-Salamó I, Papdi C, Rigó G, Zsigmond L, Vilela B, Lumbreras V, Nagy I, Horváth B, Domoki M, Darula Z, Medzihradszky K, Bögre L, Koncz C, Szabados L (2014) The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6. Plant Physiol 165:319–334PubMedPubMedCentralCrossRefGoogle Scholar
  122. Persak H, Pitzschke A (2014) Dominant repression by Arabidopsis transcription factor MYB44 causes oxidative damage and hypersensitivity to abiotic stress. Int J Mol Sci 15:2517–2537PubMedPubMedCentralCrossRefGoogle Scholar
  123. Pitzschke A, Djamei A, Bitton B, Hirt H (2009) A major role of the MEKK1–MKK1/2–MPK4 pathway in ROS signaling. Mol Plant 2:120–137PubMedPubMedCentralCrossRefGoogle Scholar
  124. Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O (2014) Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot 65:1271–1283PubMedCrossRefPubMedCentralGoogle Scholar
  125. Purvis AC (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol Plant 100:165–170CrossRefGoogle Scholar
  126. Qiao B, Zhang Q, Liu D, Wang H, Yin J, Wang R, He M, Cui M, Shang Z, Wang D, Zhu Z (2015) A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H2O2. J Exp Bot 66:5853–5866PubMedCrossRefPubMedCentralGoogle Scholar
  127. Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gaki’ere 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 death. Plant J 52:640–657PubMedCrossRefPubMedCentralGoogle Scholar
  128. 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 Environ 35:374–387PubMedCrossRefPubMedCentralGoogle Scholar
  129. Ramegowda V, Senthil-Kumar M, Nataraja KN, Reddy MK, Mysore KS, Udayakumar M (2012) Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS One 7:e40397PubMedPubMedCentralCrossRefGoogle Scholar
  130. Ramel F, Birtic S, Cuin’e S, Triantaphylid’es C, Ravanat JL, Havaux M (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158:1267–1278PubMedPubMedCentralCrossRefGoogle Scholar
  131. Rebeiz CA, Montazer-Zouhoor A, Hopen HJ, Wu SM (1984) Photodynamic herbicides: 1. Concept and phenomenology. Enzym Microb Technol 6:390–401CrossRefGoogle Scholar
  132. Rebeiz CA, Nandihalli UB, Reddy KN (1991) In: Baker NR, Percival MP (eds) Topics in Photosynthesis – volume 10, herbicides. Elsevier, Amsterdam, pp 173–208Google Scholar
  133. Rebeiz CA, Montazer-Zouhoor A, Mayasich JM, Tripathy BC, Wu SM, Rebeiz CC (1998) Photodynamic herbicides. Recent development and molecular basis of selectivity. CRC Crit Rev Plant Sci 6:385–436CrossRefGoogle Scholar
  134. Roos G, Messens J (2011) Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic Biol Med 51:314–326PubMedCrossRefGoogle Scholar
  135. Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ, Mewett OP, Howell KA, Whelan J, Kazan K, Pogson BJ (2007) Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 19:4091–4110PubMedPubMedCentralCrossRefGoogle Scholar
  136. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616–628PubMedPubMedCentralCrossRefGoogle Scholar
  137. Sato Y, Masuta Y, Saito K, Murayama S, Ozawa K (2011) Enhanced chilling tolerance at the booting stage in rice by transgenic overexpression of the ascorbate peroxidase gene, OsAPXa. Plant Cell Rep 30:399–406PubMedCrossRefGoogle Scholar
  138. Sewelam N, Jaspert N, Van Der Kelen K, Tognetti V, Schmitz J, Frerigmann H, Stahl E, Zeier J, Van Breusegem F, Maurino VG (2014) Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol Plant 7:1191–1210PubMedCrossRefGoogle Scholar
  139. Shalygo NV, Mock HP, Averina NG, Grimm B (1998) Photodynamic action of uroporphyrin and protochlorophyllide in greening barley leaves treated with cesium chloride. J Photochem Photobiol 42:151–158CrossRefGoogle Scholar
  140. Shukla D, Huda KM, Banu MS, Gill SS, Tuteja R, Tuteja N (2014) OsACA6, a P-type 2B Ca2+ ATPase functions in cadmium stress tolerance in tobacco by reducing the oxidative stress load. Planta 240:809–824PubMedCrossRefGoogle Scholar
  141. Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986PubMedCrossRefGoogle Scholar
  142. Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2:477PubMedCrossRefGoogle Scholar
  143. 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 14:691–699PubMedCrossRefGoogle Scholar
  144. Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo X, Shah J, Schlauch K, Shulaev V, Mittler R (2013) Temporal–spatial interaction between ROS and ABA controls rapid systemic acclimation in plants. Plant Cell 25:3553–3569PubMedPubMedCentralCrossRefGoogle Scholar
  145. Sweetlove LJ, Fell D, Fernie AR (2008) Getting to grips with the plant metabolic network. Biochem J 409:27–41PubMedCrossRefGoogle Scholar
  146. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244PubMedCrossRefGoogle Scholar
  147. Tamaoki M (2008) The role of phytohormone signaling in ozone-induced cell death in plants. Plant Signal Behav 3:166–174PubMedPubMedCentralCrossRefGoogle Scholar
  148. Tarrago L, Laugier E, Rey P (2009) Protein-repairing methionine sulfoxide reductases in photosynthetic organisms: gene organization, reduction mechanisms, and physiological roles. Mol Plant 2:202–217PubMedCrossRefGoogle Scholar
  149. Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inzé D, Van Breusegem F (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates arabidopsis architecture and water stress tolerance[W]. Plant Cell 22:2660–2679PubMedPubMedCentralCrossRefGoogle Scholar
  150. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403PubMedPubMedCentralCrossRefGoogle Scholar
  151. Triantaphylidès C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968PubMedPubMedCentralCrossRefGoogle Scholar
  152. Tripathy BC, Chakraborty N (1991) 5-Aminolevulinic acid induced photodynamic damage of the photosynthetic electron transport chain of cucumber (Cucumis sativus L.) cotyledons. Plant Physiol 96:761–767PubMedPubMedCentralCrossRefGoogle Scholar
  153. Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633PubMedPubMedCentralCrossRefGoogle Scholar
  154. Tripathy BC, Mohapatra A, Gupta I (2007) Impairment of the photosynthetic apparatus by oxidative stress induced by photosensitization reaction of protoporphyrin IX. Biochim Biophys Acta 1767:860–868PubMedCrossRefGoogle Scholar
  155. Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L.cv.IR64). Plant J 76:115–127PubMedGoogle Scholar
  156. Uchida A, Andre T, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523CrossRefGoogle Scholar
  157. Vainonen JP, Kangasjärvi K (2015) Plant signalling in acute ozone exposure. Plant Cell Environ 38:240–252PubMedCrossRefGoogle Scholar
  158. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821PubMedPubMedCentralCrossRefGoogle Scholar
  159. Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J, Dietz KJ (2014) Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell 26:1151–1165PubMedPubMedCentralCrossRefGoogle Scholar
  160. Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294PubMedCrossRefGoogle Scholar
  161. Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107PubMedCrossRefGoogle Scholar
  162. Wang P, Du Y, Zhao X, Miao CP, Song Y (2013) The MPK6-ERF6-ROS-responsive cis-acting Element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol 161:1392–1408PubMedPubMedCentralCrossRefGoogle Scholar
  163. Wang F, Chen HW, Li QT, Wei W, Li W, Zhang WK, Ma B, Bi YD, Lai YC, Liu XL, Man WQ, Zhang JS, Chen SY (2015) GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. Plant J 83:224–236PubMedCrossRefGoogle Scholar
  164. Wang Y, Lyu W, Berkowitz O, Radomiljac JD, Law SR, Murcha MW, Carrie C, Teixeira PF, Kmiec B, Duncan O, Van Aken O, Narsai R, Glaser E, Huang S, Roessner U, Millar AH, Whelan J (2016) Inactivation of mitochondrial complex I induces the expression of a twin cysteine protein that targets and affects cytosolic, chloroplastidic and mitochondrial function. Mol Plant 9:696–710PubMedCrossRefGoogle Scholar
  165. Waszczak C, Akter S, Eeckhout D, Persiau G, Wahni K, Bodra N, Van Molle I, De Smet B, Vertommen D, Gevaert K, De Jaeger G, Van Montagu M, Messens J, Van Breusegem F (2014) Sulfenome mining in Arabidopsis thaliana. Proc Natl Acad Sci U S A 111:11545–11550PubMedPubMedCentralCrossRefGoogle Scholar
  166. 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
  167. Waszczak C, Carmody M, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69:209–236PubMedCrossRefGoogle Scholar
  168. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamoto K (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022–4034PubMedPubMedCentralCrossRefGoogle Scholar
  169. Wood ZA, Poole LB, Karplus PA (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650–653PubMedCrossRefGoogle Scholar
  170. Wrzaczek M, Vainonen JP, Stael S, Tsiatsiani L, Help-Rinta-Rahko H, Gauthier A, Kaufholdt D, Bollhöner B, Lamminmäki A, Staes A, Gevaert K, Tuominen H, Van Breusegem F, Helariutta Y, Kangasjärvi J (2015) GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis. EMBO J 34:55–66PubMedCrossRefGoogle Scholar
  171. Wu J, Sun Y, Zhao Y, Zhang J, Luo L, Li M, Wang J, Yu H, Liu G, Yang L, Xiong G, Zhou JM, Zuo J, Wang Y, Li J (2015) Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species. Cell Res 25:621–633PubMedPubMedCentralCrossRefGoogle Scholar
  172. Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814PubMedPubMedCentralCrossRefGoogle Scholar
  173. Xing Y, Jia W, Zhang J (2007) AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J Exp Bot 58:2969–2981PubMedCrossRefGoogle Scholar
  174. Yi SY, Lee DJ, Yeom SI, Yoon J, Kim YH, Kwon SY, Choi D (2010) A novel pepper (Capsicum annuum) receptor-like kinase functions as a negative regulator of plant cell death via accumulation of superoxide anions. New Phytol 185:701–715PubMedCrossRefGoogle Scholar
  175. Yoshida K, Hisabori T (2014) Mitochondrial isocitrate dehydrogenase is inactivated upon oxidation and reactivated by thioredoxin-dependent reduction in Arabidopsis. Front Environ Sci 2:38CrossRefGoogle Scholar
  176. Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol 54:875–892PubMedCrossRefGoogle Scholar
  177. You J, Hu H, Xiong L (2012) An ornithine delta-amino transferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci 197:59–69PubMedCrossRefGoogle Scholar
  178. You J, Zong W, Li X, Ning J, Hu H, Xiao J, Xiong L (2013) The SNAC1- targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64:569–583PubMedCrossRefGoogle Scholar
  179. You J, Zong W, Hu H, Li X, Xiao J, Xiong L (2014) A STRESS- RESPONSIVE NAC1-regulated protein phosphatase gene rice protein phosphatase18 modulates drought and oxidative stress tolerance through abscisic acid-independent reactive oxygen species scavenging in rice. Plant Physiol 166:2100–2114PubMedPubMedCentralCrossRefGoogle Scholar
  180. Zhang Y, Tan J, Guo Z, Lu S, He S, Shu W, Zhou B (2009a) Increased abscisic acid levels in transgenic tobacco over-expressing 9cis-epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant Cell Environ 32:509–519PubMedCrossRefGoogle Scholar
  181. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009b) Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377PubMedPubMedCentralCrossRefGoogle Scholar
  182. Zhang CJ, Zhao BC, Ge WN, Zhang YF, Song Y, Sun DY, Guo Y (2011) An apoplastic h-type thioredoxin is involved in the stress response through regulation of the apoplastic reactive oxygen species in rice. Plant Physiol 157:1884–1899PubMedPubMedCentralCrossRefGoogle Scholar
  183. Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Ba H, Zhou J, Zhang Y (2012) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11:253–263PubMedCrossRefGoogle Scholar
  184. Zhang S, Zhang D, Yang C (2014) AtFtsH4 perturbs the mitochondrial respiratory chain complexes and auxin homeostasis in Arabidopsis. Plant Signal Behav 9:e29709PubMedPubMedCentralCrossRefGoogle Scholar
  185. Zhou G, Qi J, Ren N, Cheng J, Erb M, Mao B, Lou Y (2009) Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–648PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Mrinalini Manna
    • 1
  • V. Mohan M. Achary
    • 1
  • Malireddy K. Reddy
    • 1
    Email author
  1. 1.International Centre for Genetic Engineering and BiotechnologyNew DelhiIndia

Personalised recommendations