Skip to main content

Stress Signaling III: Reactive Oxygen Species (ROS)

  • Chapter
  • First Online:
Abiotic Stress Adaptation in Plants

Summary

Previously regarded merely as damaging agents, reactive oxygen species (ROS) are now understood as important signal molecules vital to normal plant growth. This tutorial review covers the emerging view of ROS signaling networks from ROS production to specific outputs. The chemical nature of individual reactive oxygen species, their site of the production, control of ROS accumulation via scavenging and detoxification, and the signaling components that interact with ROS are all inputs that are integrated to produce a specific response. ROS perception in plants remains largely undefined. However, a few mechanisms known in plants or suggested in other organisms are discussed. Using genetic and genomic tools, some of the components involved in ROS signal transduction have begun to be delineated. Transcript profiling in the model plant Arabidopsis thaliana has revealed that ROS has a large impact on the transcriptome, and that different ROS species can have common, distinct or even negative interference with each other in regulating gene expression.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

1O2 :

singlet oxygen

ABA:

abscisic acid

AOX:

alternative oxidase

APX:

ascorbate peroxidase

AsA:

ascorbic acid

CAT:

catalase

CRY1:

cryptochrome 1

DHA:

dehydroascorbic acid

GPX:

glutathione peroxidase

GR:

glutathione reductase

GSH:

glutathione (reduced)

GSSG:

glutathione (oxidized)

H2O2 :

hydrogen peroxide

HSP:

heat shock protein

JA:

jasmonic acid

LOX:

lipoxygenase

MV:

methyl viologen (paraquat)

MAPK:

mitogen-activated protein kinase

MDHA:

monodehydroascorbic acid

OH:

hydroxyl radical

·O2 -:

superoxide

O3 -:

ozone

PCD:

programmed cell death

PM:

plasma membrane

PP2C:

protein phosphatase 2C

PRX:

peroxiredoxin

PS I:

Photosystem I

PS II:

Photosystem II

RBOHs:

respiratory burst oxidase homologs

ROS:

reactive oxygen species

Rubisco:

ribulose-1,5-bisphosphate carboxylase /oxygenase

SA:

salicylic acid

SAR:

systemic acquired resistance

SOD:

superoxide dismutase

TRX:

thioredoxin

References

  • Agrawal GK, Iwahashi I, Rakwal R (2003) Small GTPase ‘Rop’: molecular switch for plant defense responses. FEBS Lett 546:173-180

    Article  PubMed  CAS  Google Scholar 

  • 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 40:512-522

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373-399

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347-356

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen’s and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601-639

    Article  PubMed  CAS  Google Scholar 

  • Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and defense gene expression in Arabidopsis. Plant Cell 16:2448-2462

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Gomez F, Martinez DE, Guiamet JJ (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). J Exp Bot 55:1663-1669

    Article  PubMed  CAS  Google Scholar 

  • Baxter-Burrell A, Yang ZB, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026-2028

    Article  PubMed  CAS  Google Scholar 

  • Berger S, Weichert H, Porzel A, Wasternack C, Kuhn H, Feussner I (2001) Enzymatic and non-enzymatic lipid peroxidation in leaf development. Biochim Biophys Acta 1533:266-276

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187-220

    Article  PubMed  CAS  Google Scholar 

  • Coego A, Ramirez V, Gil MJ, Flors V, Mauch-Mani B, Vera P (2005) An Arabidopsis homeodomain transcription factor, over-expressor of cationic peroxidase-3, mediates resistance to infection by necrotrophic pathogens. Plant Cell 17:2123-2137

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, Del Rio LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145-150

    Article  PubMed  CAS  Google Scholar 

  • Danon A, Coll NS, Apel K (2006) Cryptochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis. Proc Natl Acad Sci USA 103:17036-17041

    Article  PubMed  CAS  Google Scholar 

  • Davletova S, Rizhsky L, Liang HJ, Zhong SQ, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005a) Cytosolic ascorbate peroxidase-1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268-281

    Article  PubMed  CAS  Google Scholar 

  • 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 thaliana. Plant Physiol 139:847-856

    Article  PubMed  CAS  Google Scholar 

  • Despres C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181-2191

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697-1709

    Article  PubMed  CAS  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM, Knight MR (2005) ROS perception in Arabidopsis thaliana : the ozone-induced calcium response. Plant J 41:615-626

    Article  PubMed  CAS  Google Scholar 

  • Feng W, Liu G, Allen PD, Pessah IN (2000) Transmembrane redox sensor of ryanodine receptor complex. J Biol Chem 275:35902-35907

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866-1875

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiol Plant 100:241-254

    Article  CAS  Google Scholar 

  • Fukamatsu Y, Yabe N, Hasunuma K (2003) Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982-989

    Article  PubMed  CAS  Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436-445

    Article  PubMed  CAS  Google Scholar 

  • Geisler M, Kleczkowski LA, Karpinski S (2006) A universal algorithm for genome-wide in silico identification of biologically significant gene promoter putative cis-regulatory-elements; identification of new elements for reactive oxygen species and sucrose signaling in Arabidopsis. Plant J 45:384-398

    Article  PubMed  CAS  Google Scholar 

  • Harndahl U, Hall RB, Osteryoung KW, Vierling E, Bornman JF, Sundby C (1999) The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. Cell Stress Chaperones 4:129-138

    Article  PubMed  CAS  Google Scholar 

  • Hideg É, Barta C, Kalai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photo-inhibition or UV radiation. Plant Cell Physiol 43:1154-1164

    Article  PubMed  CAS  Google Scholar 

  • Higo TW, Hattori MG, Nakamura TPD, Natsume T, Michikawa T, Mikoshiba KIN (2005) Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44complex. Cell 120:85-98

    Article  PubMed  CAS  Google Scholar 

  • Iqbal A, Yabuta Y, Takeda T, Nakano Y, Shigeoka S (2006) Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana. FEBS J 273:5589-5597

    Article  PubMed  CAS  Google Scholar 

  • Joo JH, Wang SY, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957-970

    Article  PubMed  CAS  Google Scholar 

  • Kanwischer M, Porfirova S, Bergmuller E, Dormann P (2005) Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition and oxidative stress. Plant Physiol 137:713-723

    Article  PubMed  CAS  Google Scholar 

  • Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17:282-294

    Article  PubMed  CAS  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347-363

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623-2633

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermo-tolerance. Plant Physiol 138:882-897

    Article  PubMed  CAS  Google Scholar 

  • Lee JS, Ellis BE (2007) Arabidopsis MAPK phosphatase MKP2 positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 mitogen-activated protein kinases. J Biol Chem 282:25020-25029

    Article  PubMed  CAS  Google Scholar 

  • Ma S, Bohnert HJ (2007) Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures and cell-specific expression. Genome Biol 8:R49

    Article  Google Scholar 

  • Mahalingam R, Shah N, Scrymgeour A, Fedoroff N (2005) Temporal evolution of the Arabidopsis oxidative stress response. Plant Mol Biol 57:709-730

    Article  PubMed  CAS  Google Scholar 

  • Marchand C, Le MP, Meyer Y, Decottignies P (2006) Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics 6:6528-6537

    Article  PubMed  CAS  Google Scholar 

  • Martinsuo P, Pursiheimo S, Aro EM, Rintamäki E (2003) Dithiol oxidant and disulfide reductant dynamically regulate the phosphorylation of light-harvesting complex II proteins in thylakoid membranes. Plant Physiol 133:37-46

    Article  PubMed  CAS  Google Scholar 

  • Mason JT, Kim SK, Knaff DB, Wood MJ (2006) Thermodynamic basis for redox regulation of the Yap1 signal transduction pathway. Biochemistry 45:13409-13417

    Article  PubMed  CAS  Google Scholar 

  • Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271-8276

    Article  PubMed  CAS  Google Scholar 

  • Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signaling. Planta 214:775-782

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853-867

    PubMed  CAS  Google Scholar 

  • Miao Y, Laun TM, Smykowski A, Zentgraf U (2007) Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol Biol 65:63-76

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279-288

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490-498

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Kim Y, Song LH, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537-6542

    Article  PubMed  CAS  Google Scholar 

  • Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459-481

    Article  PubMed  Google Scholar 

  • 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 281:38697-38704

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, De PR, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125-134

    Article  PubMed  CAS  Google Scholar 

  • 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 15:2320-2332

    Google Scholar 

  • Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335-342

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Ormrod DP (1995) Impact of Uvb and O-3 on the oxygen-free radical scavenging system in Arabidopsis thaliana genotypes differing in flavonoid biosynthesis. Photochem Photobiol 62:719-726

    Article  CAS  Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858-861

    Article  PubMed  CAS  Google Scholar 

  • Rizhsky L, Liang H, Mittler R (2003) The water-water cycle is essential for chloroplast protection in the absence of stress. J Biol Chem 278:38921-38925

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Jacquot JP (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74:259-268

    Article  PubMed  CAS  Google Scholar 

  • 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 16:616-628

    Article  PubMed  CAS  Google Scholar 

  • Samuel MA, Miles GP, Ellis BE (2000) Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J 22:367-376

    Article  PubMed  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995-1014

    Article  PubMed  CAS  Google Scholar 

  • Schubert R, Fischer R, Hain R, Schreier PH, Bahnweg G, Ernst D, Sandermann H (1997) An ozone-responsive region of the grapevine resveratrol synthase promoter differs from the basal pathogen-responsive sequence. Plant Mol Biol 34:417-426

    Article  PubMed  CAS  Google Scholar 

  • Shao N, Krieger-Liszkay A, Schroda M, Beck CF (2007) A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J 50:475-487

    Article  PubMed  CAS  Google Scholar 

  • Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci USA 103:19587-19592

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tosti N, Pasqualini S, Borgogni A, Ederli L, Falistocco E, Crispi S, Paolocci F (2006) Gene expression profiles of O3-treated Arabidopsis plants. Plant Cell Environ 29:1686-1702

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto S, Morita S, Hirano E, Yokoi H, Masumura T, Tanaka K (2005) A novel cis-element that is responsive to oxidative stress regulates three antioxidant defense genes in rice. Plant Physiol 137:317-327

    Article  PubMed  CAS  Google Scholar 

  • Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45-58

    Article  PubMed  CAS  Google Scholar 

  • 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 139:806-821

    Article  PubMed  CAS  Google Scholar 

  • Vollenweider S, Weber H, Stolz S, Chetelat A, Farmer EE (2000) Fatty acid ketodienes and fatty acid ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves. Plant J 24:467-476

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg É, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183-1185

    Article  PubMed  CAS  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inze D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. EMBO J 16:4806-4816

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The funding sources acknowledged for this work are: Finnish Academy Centre of Excellence program (2006-2011) and research grant to JK (decision # 121576), Post-doctoral grants to KO (decision # 115034) and MB (decision # 108760). MW is supported by a Helsinki University Post-doctoral grant.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Additional information

# Equal contribution

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Brosché, M., Overmyer, K., Wrzaczek, M., Kangasjärvi, J., Kangasjärvi, S. (2009). Stress Signaling III: Reactive Oxygen Species (ROS). In: Pareek, A., Sopory, S., Bohnert, H. (eds) Abiotic Stress Adaptation in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3112-9_5

Download citation

Publish with us

Policies and ethics