Advertisement

ROS as Key Players of Abiotic Stress Responses in Plants

  • Nobuhiro SuzukiEmail author

Abstract

Despite their toxic potential, reactive oxygen species (ROS) play an integral role as signaling molecules in the regulation of a broad range of biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants. To some extent, various functions of ROS signaling are attributed to differences in the regulatory mechanisms of respiratory burst oxidase homologs (RBOHs) that are involved in a multitude of different signal transduction pathways activated in assorted tissue and cell types under fluctuating environmental conditions. To acclimate or survive under abiotic stress conditions, plants possess powerful strategies involving systemic signaling, retrograde signaling, and programmed cell death (PCD), in which ROS signals are integrated with other pathways to generate highly coordinated signaling networks. In this chapter, beneficial roles of ROS as signaling molecules in the regulation of abiotic stress responses in plants will be addressed.

Keywords

Abiotic stress Hormones NADPH oxidase Programmed cell death Redox signaling ROS signal Systemic signaling Retrograde signaling 

Abbreviations

ABA

Abscisic acid

ABI4

ABA-insensitive 4

ACC

1-Aminocyclopropane-1-carboxylic acid

ANAC017

A membrane-bound NAC 017

AOX

Alternative oxidase

APX

Ascorbate peroxidase

BCL2

B-cell lymphoma 2

BR

Brassinosteroid

CDPKs

Calcium-dependent protein kinases

CTR1

Constitutive triple response 1

DPI

Diphenyleneiodonium

EDS1

Enhanced disease susceptibility 1

EIN2

Ethylene-insensitive 2

EEE

Excess excitation energy

GUN1

Genomes uncoupled 1

IAA

Indole-3-acetic acid

JA

Jasmonic acid

LSD1

Lesion simulating disease 1

MAPK

Mitogen-activated protein kinase

NPQ

Non-photochemical quenching

MeJA

Methyl jasmonate

OST1

Open stomata 1

PA

Phosphatidic acid

PCD

Programmed cell death

PAD4

Phytoalexin-deficient 4

PRL1

Pleiotropic response locus 1

PQ

Plastoquinone

RBOH

Respiratory burst oxidase homolog

ROS

Reactive oxygen species

SA

Salicylic acid

SAA

Systemic acquired acclimation

SAR

Systemic acquired resistance

SID2

Salicylic acid induction deficient 2

TPC1

Two-pore channel 1

VPE

Vacuolar processing enzymes

Notes

Acknowledgment

This work was supported by funding from Sophia University in Japan.

References

  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  2. Araya T, Noguchi K, Terashima I (2008) Manipulation of light and CO2 environments of the primary leaves of bean (Phaseolus vulgaris L.) affects photosynthesis in both the primary and the first trifoliate leaves: involvement of systemic regulation. Plant Cell Environ 31:50–61PubMedGoogle Scholar
  3. Bandurska H, Niedziela J, Chadzinikolau T (2013) Separate and combined responses to water deficit and UV-B radiation. Plant Sci Int J Exp Plant Biol 213:98–105Google Scholar
  4. Baruah A, Simkova K, Hincha DK, Apel K, Laloi C (2009) Modulation of O-mediated retrograde signaling by the PLEIOTROPIC RESPONSE LOCUS 1 (PRL1) protein, a central integrator of stress and energy signaling. Plant J Cell Mol Biol 60:22–32CrossRefGoogle Scholar
  5. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240PubMedCrossRefGoogle Scholar
  6. Benschop JJ, Mohammed S, O’Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214PubMedCrossRefGoogle Scholar
  7. Bienert GP, Schjoerring JK, Jahn TP (2006) Membrane transport of hydrogen peroxide. Biochim Biophys Acta 1758:994–1003PubMedCrossRefGoogle Scholar
  8. Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192PubMedCrossRefGoogle Scholar
  9. Carr JP, Lewsey MG, Palukaitis P (2010) Signaling in induced resistance. Adv Virus Res 76:57–121PubMedCrossRefGoogle Scholar
  10. Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111:6497–6502PubMedCentralPubMedCrossRefGoogle Scholar
  11. Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8:e23681PubMedCrossRefGoogle Scholar
  12. Coll NS, Danon A, Meurer J, Cho WK, Apel K (2009) Characterization of soldat8, a suppressor of singlet oxygen-induced cell death in Arabidopsis seedlings. Plant Cell Physiol 50:707–718PubMedCrossRefGoogle Scholar
  13. Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K, Woodward FI, Gray JE, Quick WP (2006) Systemic signalling of environmental cues in Arabidopsis leaves. J Exp Bot 57:329–341PubMedCrossRefGoogle Scholar
  14. Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287PubMedCentralPubMedCrossRefGoogle Scholar
  15. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123:1468–1479PubMedCrossRefGoogle Scholar
  16. Dempsey DA, Klessig DF (2012) SOS - too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545PubMedCrossRefGoogle Scholar
  17. Doyle SM, McCabe PF (2010) Type and cellular location of reactive oxygen species determine activation or suppression of programmed cell death in Arabidopsis suspension cultures. Plant Signal Behav 5:467–468PubMedCrossRefGoogle Scholar
  18. 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 6:559–569PubMedCrossRefGoogle Scholar
  19. Duan Y, Zhang W, Li B, Wang Y, Li K, Sodmergen, Han C, Zhang Y, Li X (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytol 186:681–695PubMedCrossRefGoogle Scholar
  20. 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 USA 110:8744–8749PubMedCentralPubMedCrossRefGoogle Scholar
  21. Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signalling molecule H2O2. Biochem J 414:53–61PubMedCrossRefGoogle Scholar
  22. Finka A, Cuendet AF, Maathuis FJ, Saidi Y, Goloubinoff P (2012) Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell 24:3333–3348PubMedCentralPubMedCrossRefGoogle Scholar
  23. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18PubMedCentralPubMedCrossRefGoogle Scholar
  24. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  25. 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 signaling in Arabidopsis. Plant Physiol 141:436–445PubMedCentralPubMedCrossRefGoogle Scholar
  26. Galvez-Valdivieso G, Mullineaux PM (2010) The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol Plant 138:430–439PubMedCrossRefGoogle Scholar
  27. Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D (2012) Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol Life Sci 69:3175–3186PubMedCrossRefGoogle Scholar
  28. Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630PubMedCrossRefGoogle Scholar
  29. Giraud E, Van Aken O, Ho LH, Whelan J (2009) The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol 150:1286–1296PubMedCentralPubMedCrossRefGoogle Scholar
  30. Glauser G, Dubugnon L, Mousavi SA, Rudaz S, Wolfender JL, Farmer EE (2009) Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J Biol Chem 284:34506–34513PubMedCentralPubMedCrossRefGoogle Scholar
  31. Gordon MJ, Carmody M, Albrecht V, Pogson B (2012) Systemic and local responses to repeated HL stress-induced retrograde signaling in Arabidopsis. Front Plant Sci 3:303PubMedCentralPubMedGoogle Scholar
  32. Gorsuch PA, Sargeant AW, Penfield SD, Quick WP, Atkin OK (2010) Systemic low temperature signaling in Arabidopsis. Plant Cell Physiol 51:1488–1498PubMedCrossRefGoogle Scholar
  33. Gunawardena A, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214PubMedCrossRefGoogle Scholar
  34. Huang X, Li Y, Zhang X, Zuo J, Yang S (2010) The Arabidopsis LSD1 gene plays an important role in the regulation of low temperature-dependent cell death. New Phytol 187:301–312PubMedCrossRefGoogle Scholar
  35. Huh GH, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J Cell Mol Biol 29:649–659CrossRefGoogle Scholar
  36. Iglesias MJ, Terrile MC, Bartoli CG, D’Ippolito S, Casalongue CA (2010) Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol 74:215–222PubMedCrossRefGoogle Scholar
  37. Ismail A, Takeda S, Nick P (2014) Life and death under salt stress: same players, different timing? J Exp Bot 65:2963–2979PubMedCrossRefGoogle Scholar
  38. Jakubowicz M, Galganska H, Nowak W, Sadowski J (2010) Exogenously induced expression of ethylene biosynthesis, ethylene perception, phospholipase D, and Rboh-oxidase genes in broccoli seedlings. J Exp Bot 61:3475–3491PubMedCentralPubMedCrossRefGoogle Scholar
  39. 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 USA 106:20520–20525PubMedCentralPubMedCrossRefGoogle Scholar
  40. Jaspers P, Kangasjarvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413PubMedCrossRefGoogle Scholar
  41. Jia L (2011) Is reactive oxygen species (ROS) the underlying factor for inhibited root growth in Osspr1? Plant Signal Behav 6:1024–1025PubMedCrossRefGoogle Scholar
  42. Jiang C, Belfield EJ, Mithani A, Visscher A, Ragoussis J, Mott R, Smith JA, Harberd NP (2012) ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J 31:4359–4370PubMedCentralPubMedCrossRefGoogle Scholar
  43. Kalachova T, Iakovenko O, Kretinin S, Kravets V (2013) Involvement of phospholipase D and NADPH-oxidase in salicylic acid signaling cascade. Plant Physiol Biochem 66:127–133PubMedCrossRefGoogle Scholar
  44. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657PubMedCrossRefGoogle Scholar
  45. Karpinski S, Szechynska-Hebda M, Wituszynska W, Burdiak P (2013) Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ 36:736–744PubMedCrossRefGoogle Scholar
  46. Kerchev PI, Pellny TK, Vivancos PD, Kiddle G, Hedden P, Driscoll S, Vanacker H, Verrier P, Hancock RD, Foyer CH (2011) The transcription factor ABI4 Is required for the ascorbic acid-dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. Plant Cell 23:3319–3334PubMedCentralPubMedCrossRefGoogle Scholar
  47. Khokon MA, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2010) Yeast elicitor-induced stomatal closure and peroxidase-mediated ROS production in Arabidopsis. Plant Cell Physiol 51:1915–1921PubMedCrossRefGoogle Scholar
  48. Khokon AR, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environ 34:434–443PubMedCrossRefGoogle Scholar
  49. Kim MJ, Ciani S, Schachtman DP (2010) A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. Mol Plant 3:420–427PubMedCrossRefGoogle Scholar
  50. Kim Y, Wang M, Bai Y, Zeng Z, Guo F, Han N, Bian H, Wang J, Pan J, Zhu M (2014) Bcl-2 suppresses activation of VPEs by inhibiting cytosolic Ca(2)(+) level with elevated K(+) efflux in NaCl-induced PCD in rice. Plant Physiol Biochem 80:168–175PubMedCrossRefGoogle Scholar
  51. 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 Mol Cell Res 1823:398–405CrossRefGoogle Scholar
  52. 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 19:1065–1080PubMedCentralPubMedCrossRefGoogle Scholar
  53. Koo AJ, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J Cell Mol Biol 59:974–986CrossRefGoogle Scholar
  54. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719PubMedCrossRefGoogle Scholar
  55. Krishnamurthy A, Rathinasabapathi B (2013a) Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant Cell Environ 36:1838–1849PubMedCrossRefGoogle Scholar
  56. Krishnamurthy A, Rathinasabapathi B (2013b) Oxidative stress tolerance in plants: novel interplay between auxin and reactive oxygen species signaling. Plant Signal Behav. doi: 10.4161/psb.25761 PubMedCentralPubMedGoogle Scholar
  57. Kunihiro S, Hiramatsu T, Kawano T (2011) Involvement of salicylic acid signal transduction in aluminum-responsive oxidative burst in Arabidopsis thaliana cell suspension culture. Plant Signal Behav 6:611–616PubMedCentralPubMedCrossRefGoogle Scholar
  58. 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 22:2623–2633PubMedCentralPubMedCrossRefGoogle Scholar
  59. Kwasniewski M, Chwialkowska K, Kwasniewska J, Kusak J, Siwinski K, Szarejko I (2013) Accumulation of peroxidase-related reactive oxygen species in trichoblasts correlates with root hair initiation in barley. J Plant Physiol 170:185–195PubMedCrossRefGoogle Scholar
  60. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:672–677PubMedCentralPubMedCrossRefGoogle Scholar
  61. 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 USA 104:10270–10275PubMedCentralPubMedCrossRefGoogle Scholar
  62. Leon J (2013) Role of plant peroxisomes in the production of jasmonic acid-based signals. Subcell Biochem 69:299–313PubMedCrossRefGoogle Scholar
  63. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260PubMedCrossRefGoogle Scholar
  64. Li Z, Yue H, Xing D (2012) MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol 195:85–96PubMedCrossRefGoogle Scholar
  65. Li P, Chen L, Zhou Y, Xia X, Shi K, Chen Z, Yu J (2013a) Brassinosteroids-induced systemic stress tolerance was associated with increased transcripts of several defence-related genes in the phloem in. PLoS One 8:e66582PubMedCentralPubMedCrossRefGoogle Scholar
  66. Li Y, Chen L, Mu J, Zuo J (2013b) LESION SIMULATING DISEASE1 interacts with catalases to regulate hypersensitive cell death in Arabidopsis. Plant Physiol 163:1059–1070PubMedCentralPubMedCrossRefGoogle Scholar
  67. 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 60:3221–3238PubMedCentralPubMedCrossRefGoogle Scholar
  68. Liu YH, Offler CE, Ruan YL (2013) Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals. Front Plant Sci 4:282PubMedCentralPubMedGoogle Scholar
  69. Lv WT, Lin B, Zhang M, Hua XJ (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933PubMedCentralPubMedCrossRefGoogle Scholar
  70. 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
  71. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15PubMedCrossRefGoogle Scholar
  72. Maruta T, Inoue T, Noshi M, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012) Cytosolic ascorbate peroxidase 1 protects organelles against oxidative stress by wounding- and jasmonate-induced H(2)O(2) in Arabidopsis plants. Biochim Biophys Acta 1820:1901–1907PubMedCrossRefGoogle Scholar
  73. 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
  74. Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009a) Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J Biol Chem 284:26482–26492PubMedCentralPubMedCrossRefGoogle Scholar
  75. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009b) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45PubMedGoogle Scholar
  76. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  77. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  78. 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
  79. Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 73:91–104PubMedCrossRefGoogle Scholar
  80. Moller IM, Sweetlove LJ (2010) ROS signalling–specificity is required. Trends Plant Sci 15:370–374PubMedCrossRefGoogle Scholar
  81. Monetti E, Kadono T, Tran D, Azzarello E, Arbelet-Bonnin D, Biligui B, Briand J, Kawano T, Mancuso S, Bouteau F (2014) Deciphering early events involved in hyperosmotic stress-induced programmed cell death in tobacco BY-2 cells. J Exp Bot 65:1361–1375PubMedCentralPubMedCrossRefGoogle Scholar
  82. 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 USA 104:20996–21001PubMedCentralPubMedCrossRefGoogle Scholar
  83. Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21:2341–2356PubMedCentralPubMedCrossRefGoogle Scholar
  84. Montillet JL, Hirt H (2013) New checkpoints in stomatal defense. Trends Plant Sci 18:295–297PubMedCrossRefGoogle Scholar
  85. Mori IC, Pinontoan R, Kawano T, Muto S (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol 42:1383–1388PubMedCrossRefGoogle Scholar
  86. 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 20:2339–2356PubMedCentralPubMedCrossRefGoogle Scholar
  87. Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48PubMedCrossRefGoogle Scholar
  88. Munn-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216CrossRefGoogle Scholar
  89. Nakagami H, Soukupova H, Schikora A, Zarsky V, Hirt H (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281:38697–38704PubMedCrossRefGoogle Scholar
  90. 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 25:3450–3471PubMedCentralPubMedCrossRefGoogle Scholar
  91. Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. Plant J Cell Mol Biol 61:1053–1066CrossRefGoogle Scholar
  92. O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779PubMedCrossRefGoogle Scholar
  93. 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 285:1435–1445PubMedCentralPubMedCrossRefGoogle Scholar
  94. Oelze ML, Vogel MO, Alsharafa K, Kahmann U, Viehhauser A, Maurino VG, Dietz KJ (2012) Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10- or 100-fold light increment and the possible involvement of retrograde signals. J Exp Bot 63:1297–1313PubMedCentralPubMedCrossRefGoogle Scholar
  95. 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 283:8885–8892PubMedCrossRefGoogle Scholar
  96. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332PubMedCentralPubMedCrossRefGoogle Scholar
  97. Padmanabhan MS, Dinesh-Kumar SP (2010) All hands on deck-the role of chloroplasts, endoplasmic reticulum, and the nucleus in driving plant innate immunity. Mol Plant Microbe Interact 23:1368–1380PubMedCrossRefGoogle Scholar
  98. Peer WA, Cheng Y, Murphy AS (2013) Evidence of oxidative attenuation of auxin signalling. J Exp Bot 64:2629–2639PubMedCrossRefGoogle Scholar
  99. Petrov VD, Van Breusegem F (2012) Hydrogen peroxide-a central hub for information flow in plant cells. AoB Plants 2012:pls014PubMedCentralPubMedCrossRefGoogle Scholar
  100. Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69PubMedCentralPubMedCrossRefGoogle Scholar
  101. Pfannschmidt T (2010) Plastidial retrograde signalling–a true “plastid factor” or just metabolite signatures? Trends Plant Sci 15:427–435PubMedCrossRefGoogle Scholar
  102. Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2:120–137PubMedCentralPubMedCrossRefGoogle Scholar
  103. Pogson BJ, Woo NS, Forster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13:602–609PubMedCrossRefGoogle Scholar
  104. Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, Mackinlay J, Loake GJ, Mundy J, Morris PC (2008) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148:212–222PubMedCentralPubMedCrossRefGoogle Scholar
  105. Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M (2011) Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytol 190:351–368PubMedCrossRefGoogle Scholar
  106. Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7:177–194PubMedCrossRefGoogle Scholar
  107. 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 19:4091–4110PubMedCentralPubMedCrossRefGoogle Scholar
  108. Ruckle ME, Burgoon LD, Lawrence LA, Sinkler CA, Larkin RM (2012) Plastids are major regulators of light signaling in Arabidopsis. Plant Physiol 159:366–390PubMedCentralPubMedCrossRefGoogle Scholar
  109. 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 16:616–628PubMedCentralPubMedCrossRefGoogle Scholar
  110. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098PubMedCrossRefGoogle Scholar
  111. Shabala S, Shabala L, Barcelo J, Poschenrieder C (2014) Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ 37:2216–2233PubMedGoogle Scholar
  112. Shah J, Zeier J (2013) Long-distance communication and signal amplification in systemic acquired resistance. Front Plant Sci 4:30PubMedCentralPubMedCrossRefGoogle Scholar
  113. Shapiguzov A, Vainonen JP, Wrzaczek M, Kangasjarvi J (2012) ROS-talk-how the apoplast, the chloroplast, and the nucleus get the message through. Front Plant Sci 3:292PubMedCentralPubMedCrossRefGoogle Scholar
  114. Sierla M, Rahikainen M, Salojarvi J, Kangasjarvi J, Kangasjarvi S (2013) Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid Redox Signal 18:2220–2239PubMedCrossRefGoogle Scholar
  115. 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
  116. Soares NC, Francisco R, Vielba JM, Ricardo CP, Jackson PA (2009) Associating wound-related changes in the apoplast proteome of Medicago with early steps in the ROS signal-transduction pathway. J Proteome Res 8:2298–2309PubMedCrossRefGoogle Scholar
  117. Song Y, Miao Y, Song CP (2014) Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol 201:1121–1140PubMedCrossRefGoogle Scholar
  118. Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100PubMedCrossRefGoogle Scholar
  119. Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378PubMedCrossRefGoogle Scholar
  120. Suzuki N, Mittler R (2012) Reactive oxygen species-dependent wound responses in animals and plants. Free Radic Biol Med 53:2269–2276PubMedCrossRefGoogle Scholar
  121. 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
  122. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270PubMedCrossRefGoogle Scholar
  123. 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 reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25:3553–3569PubMedCentralPubMedCrossRefGoogle Scholar
  124. Szechynska-Hebda M, Karpinski S (2013) Light intensity-dependent retrograde signalling in higher plants. J Plant Physiol 170:1501–1516PubMedCrossRefGoogle Scholar
  125. Szechynska-Hebda M, Kruk J, Gorecka M, Karpinska B, Karpinski S (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 22:2201–2218PubMedCentralPubMedCrossRefGoogle Scholar
  126. Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 5:1370–1378PubMedCentralPubMedCrossRefGoogle Scholar
  127. Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19:805–818PubMedCentralPubMedCrossRefGoogle Scholar
  128. Takahashi F, Mizoguchi T, Yoshida R, Ichimura K, Shinozaki K (2011) Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol Cell 41:649–660PubMedCrossRefGoogle Scholar
  129. 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
  130. Teakle NL, Tyerman SD (2010) Mechanisms of Cl(-) transport contributing to salt tolerance. Plant Cell Environ 33:566–589PubMedCrossRefGoogle Scholar
  131. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152PubMedCrossRefGoogle Scholar
  132. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403PubMedCrossRefGoogle Scholar
  133. Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134PubMedCrossRefGoogle Scholar
  134. Toumi I, Moschou PN, Paschalidis KA, Bouamama B, Ben Salem-Fnayou A, Ghorbel AW, Mliki A, Roubelakis-Angelakis KA (2010) Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J Plant Physiol 167:519–525PubMedCrossRefGoogle Scholar
  135. Tripathy BC, Oelmuller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633PubMedCentralPubMedCrossRefGoogle Scholar
  136. Vacca RA, de Pinto MC, Valenti D, Passarella S, Marra E, De Gara L (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells. Plant Physiol 134:1100–1112PubMedCentralPubMedCrossRefGoogle Scholar
  137. Voothuluru P, Sharp RE (2013) Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance. J Exp Bot 64:1223–1233PubMedCrossRefGoogle Scholar
  138. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185PubMedCrossRefGoogle Scholar
  139. Wang GF, Li WQ, Li WY, Wu GL, Zhou CY, Chen KM (2013) Characterization of rice NADPH oxidase genes and their expression under various environmental conditions. Int J Mol Sci 14:9440–9458PubMedCentralPubMedCrossRefGoogle Scholar
  140. Wituszynska W, Szechynska-Hebda M, Sobczak M, Rusaczonek A, Kozlowska-Makulska A, Witon D, Karpinski S (2015) Lesion simulating disease 1 and enhanced disease susceptibility 1 differentially regulate UV-C-induced photooxidative stress signalling and programmed cell death in Arabidopsis thaliana. Plant Cell Environ 38:315–330PubMedCrossRefGoogle Scholar
  141. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395PubMedCrossRefGoogle Scholar
  142. Wrzaczek M, Brosche M, Kangasjarvi J (2013) ROS signaling loops-production, perception, regulation. Curr Opin Plant Biol 16:575–582PubMedCrossRefGoogle Scholar
  143. 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 150:801–814PubMedCentralPubMedCrossRefGoogle Scholar
  144. Xia XJ, Zhou YH, Ding J, Shi K, Asami T, Chen Z, Yu JQ (2011) Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol 191:706–720PubMedCrossRefGoogle Scholar
  145. Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J Cell Mol Biol 66:280–292CrossRefGoogle Scholar
  146. Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H, Liu G, Ren D (2008) Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem 283:26996–27006PubMedCrossRefGoogle Scholar
  147. Zeng W, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153:1188–1198PubMedCentralPubMedCrossRefGoogle Scholar
  148. Zhang HJ, Fang Q, Zhang ZG, Wang YC, Zheng XB (2009a) The role of respiratory burst oxidase homologues in elicitor-induced stomatal closure and hypersensitive response in Nicotiana benthamiana. J Exp Bot 60:3109–3122PubMedCentralPubMedCrossRefGoogle Scholar
  149. 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 21:2357–2377PubMedCentralPubMedCrossRefGoogle Scholar
  150. Zhang S, Apel K, Kim C (2014) Singlet oxygen-mediated and EXECUTER-dependent signalling and acclimation of Arabidopsis thaliana exposed to light stress. Philos Trans R Soc Lond B Biol Sci 369:20130227PubMedCentralPubMedCrossRefGoogle Scholar
  151. Zimmermann MR, Maischak H, Mithofer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol 149:1593–1600PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Materials and Life Sciences, Faculty of Science and TechnologySophia UniversityTokyoJapan

Personalised recommendations