Advertisement

The ROS Signaling Network of Cells

  • Yael Harir
  • Ron MittlerEmail author
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Reactive oxygen species (ROS) are toxic derivatives of atmospheric oxygen used by plant cells to control many different biological processes, including growth, development, and response to biotic and abiotic stimuli. Because of their toxicity, as well as their important signaling role, the steady-state level of ROS in cells is tightly regulated by a network of genes termed the “ROS gene network”. In the flowering plant Arabidopsis thaliana, the ROS gene network includes more than 150 genes that manage the level of ROS in cells. The ROS network is highly dynamic and redundant, and encodes for ROS-scavenging as well as ROS-producing proteins. Recent studies have unraveled some of the key players of the network and shed light on some of the questions related to its mode of regulation, its protective roles, and its modulation of signaling networks that control growth, development, and stress response. In this chapter we will describe some of these findings.

Keywords

Reactive Oxygen Species Reactive Oxygen Species Production NADPH Oxidase Reactive Oxygen Species Scavenge Reactive Oxygen Species Signaling 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55, 373–399.PubMedCrossRefGoogle Scholar
  2. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141, 391–396.PubMedCrossRefGoogle Scholar
  3. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arentzen CJ (eds), Photoinhibition, Elsevier, Amsterdam, pp 227–287.Google Scholar
  4. Ashtamker C, Kiss V, Sagi M, Davydov O, Fluhr R (2007) Diverse subcellular locations of cryptogein-induced reactive oxygen species production in tobacco Bright Yellow-2 cells. Plant Physiol 143, 1817–1826.PubMedCrossRefGoogle Scholar
  5. Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiol. 141, 311.PubMedCrossRefGoogle Scholar
  6. 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, 1183–1192.PubMedCrossRefGoogle Scholar
  7. Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Bolwell GP (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 47, 851–863.PubMedCrossRefGoogle Scholar
  8. Cheng NH, Liu JZ, Brock A, Nelson RS, Hirschi KD (2006) AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. J Biol Chem 281, 26280–26288.PubMedCrossRefGoogle Scholar
  9. Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145, 890–904.PubMedCrossRefGoogle Scholar
  10. 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, 9260–9268.PubMedCrossRefGoogle Scholar
  11. Corpas FJ, Palma JM, Sandalio LM, Valderrama R, Barroso JB, del Río LA (2008) Peroxisomal xanthine oxidoreductase: Characterization of the enzyme from pea (Pisum sativum L.) leaves. J Plant Physiol 165, 1319–1330.PubMedCrossRefGoogle Scholar
  12. Davletova S, Rizhsky L, Liang H, Shuman J, Shulaev V, Oliver D, Mittler, R (2005a) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of arabidopsis. Plant Cell 17, 268–281.CrossRefGoogle Scholar
  13. Davletova S, Schlauch K, Coutu J, Mittler R (2005b) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139, 847–856.CrossRefGoogle Scholar
  14. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141, 330–335.PubMedCrossRefGoogle Scholar
  15. Dietz K-J (2008) Redox signal integration: From stimulus to networks and genes. Physiol Plant 133, 459–468.PubMedCrossRefGoogle Scholar
  16. Dos Santos C, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11, 329–334.CrossRefGoogle Scholar
  17. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866–1875.PubMedCrossRefGoogle Scholar
  18. Giacomelli L, Masi A, Ripoll DR, Lee MJ, van Wijk KJ (2007) Arabidopsis thaliana deficient in two chloroplast ascorbate peroxidases shows accelerated light-induced necrosis when levels of cellular ascorbate are low. Plant Mol Biol 65, 627–644PubMedCrossRefGoogle Scholar
  19. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141, 312–322.PubMedCrossRefGoogle Scholar
  20. Halliwell B, Gutteridge JMC (1999). Free radicals in biology and medicine, 3rd Edition. Clarendon, Oxford.Google Scholar
  21. Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K, Chu C, Wang Y, Loake GJ (2008) Nitric oxide function and signalling in plant disease resistance. J Exp Bot 59, 147–154.PubMedCrossRefGoogle Scholar
  22. 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, 672–677.PubMedCrossRefGoogle Scholar
  23. Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. Proc Natl Acad Sci USA 103, 18008–18013.PubMedCrossRefGoogle Scholar
  24. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133, 481–489.PubMedCrossRefGoogle Scholar
  25. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144, 1777–1785PubMedCrossRefGoogle Scholar
  26. Mittler R, Herr EH, Orvar BL, van Camp W, Willekens H, Inze, D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc Natl Acad Sci USA 96, 14165–14170.PubMedCrossRefGoogle Scholar
  27. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7, 405–410.PubMedCrossRefGoogle Scholar
  28. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9, 490–498.PubMedCrossRefGoogle Scholar
  29. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11, 15–19.PubMedCrossRefGoogle Scholar
  30. Mittler R, Song L, Coutu J, Coutu A, Ciftci S, Kim YS, Lee H, Stevenson B, Zhu, J-K (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580, 6537–6542.PubMedCrossRefGoogle Scholar
  31. Møller IM (2001) Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52, 561–591.PubMedCrossRefGoogle Scholar
  32. 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, 20996–201001.PubMedCrossRefGoogle Scholar
  33. 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, 8885–8892.PubMedCrossRefGoogle Scholar
  34. Pnueli L, Hongjian L, Mittler R (2003) Growth suppression, abnormal guard cell response, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1) – deficient Arabidopsis plants. Plant J 34, 187–203.PubMedCrossRefGoogle Scholar
  35. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc-finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279, 11736–11743.PubMedCrossRefGoogle Scholar
  36. Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Rodermel S, Inzé D, Mittler R (2002) Double antisense plants with suppressed expression of ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants with suppressed expression of ascorbate peroxidase or catalase. Plant J 32, 329–342.PubMedCrossRefGoogle Scholar
  37. Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz K-J, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19, 4120–4130.PubMedCrossRefGoogle Scholar
  38. Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stresses in transgenic plants expressing the transcriptional co-activator MBF1. Plant Physiol 139, 1313–1322.PubMedCrossRefGoogle Scholar
  39. Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283, 9269–9275.PubMedCrossRefGoogle Scholar
  40. 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, 1241–1244.PubMedCrossRefGoogle Scholar
  41. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8, 397–403.PubMedCrossRefGoogle Scholar
  42. Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141, 373–378.PubMedCrossRefGoogle Scholar
  43. Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147, 978–984.PubMedCrossRefGoogle Scholar
  44. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31, 622–631.PubMedCrossRefGoogle Scholar
  45. 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, 4022–4034.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular BiologyUniversity of NevadaRenoNV

Personalised recommendations