Reactive Oxygen Species Metabolism in Plants: Production, Detoxification and Signaling in the Stress Response
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® Plant Stress ©2008 Global Science Books Reactive Oxygen Species Metabolism in Plants: Production, Detoxification and Signaling in the Stress Response Priscilla P. Bettini1 • Elena Cosi1,2 • Daniela Bindi1 • Marcello Buiatti1* 1 Department of Evolutionary Biology “Leo Pardi”, University of Florence, Italy 2 Present address, Center for Research in Agrobiology and Pedology, Council for Research and Experimentation in Agriculture (CRA), Cascine del Riccio (FI), Italy Corresponding author : * [email protected] ABSTRACT •- • The production of reactive oxygen species (ROS), such as superoxide radical (O2 ), hydroxyl radical (OH ) and hydrogen peroxide (H2O2), in plants is a common event in metabolic and physiological processes. ROS are normally formed in photosynthesis and respiration by the chloroplast and mitochondrial electron transfer chains, respectively, and in metabolic reactions taking place in the peroxisomes. As these active oxygen species are destructive to cellular components such as lipids, nucleic acid and proteins, plant cells are equipped with non-enzymatic and enzymatic antioxidant defense systems comprising ascorbate, glutathione, phenols, catalases, super- oxide dismutases and peroxidases. Biotic and abiotic stress, such as salinity stress, excess of heavy metals, mechanical shock, UV light, exposure to ozone, water deficiency and pathogen attack, also increase ROS production. In the latter case the release of ROS, referred to as the “oxidative burst”, is one of the earliest responses activated following pathogen recognition and has been suggested to play a pivotal role in the integration and the coordination of the plant defense responses. In this review we summarize the current knowledge about ROS production and oxidative defense in plants. The role of ROS will be discussed in the frame of stress responses, with emphasis on the plant-pathogen interaction. _____________________________________________________________________________________________________________ Keywords: abiotic stress, oxidative burst, oxygen radicals, plant-pathogen interaction, ROS, ROS signaling Abbreviations: AsA, ascorbic acid; CAT, catalase; ET, ethylene; GSH, glutathione; JA, jasmonic acid; HR, hypersensitive response; MAPK, mitogen-activated protein kinase; NADPH, nicotinamide adenine dinucleotide phosphate; NO, nitric oxide; PCD, programmed cell death; ROS, reactive oxygen species; SA, salicylic acid; SAR, systemic acquired resistance; SOD, superoxide dismutase CONTENTS INTRODUCTION........................................................................................................................................................................................ 28 ROS GENERATION AND SCAVENGING ................................................................................................................................................ 28 ROS IN THE PLANT STRESS RESPONSE............................................................................................................................................... 31 ROS in plant-pathogen interactions......................................................................................................................................................... 31 Functions of ROS in the plant defense response...................................................................................................................................... 33 ROS signal transduction .......................................................................................................................................................................... 34 ROS and abiotic stress: the response to ozone......................................................................................................................................... 35 CONCLUSIONS.......................................................................................................................................................................................... 36 ACKNOWLEDGEMENTS ......................................................................................................................................................................... 36 REFERENCES............................................................................................................................................................................................. 36 _____________________________________________________________________________________________________________ INTRODUCTION temperature extremes, excess of light, air pollutants, anoxia, heavy metals, water deficit and pathogen attack (Smirnoff The production of reactive oxygen species (ROS), also 1993; Lamb and Dixon 1997; Dat et al. 2000; Blokhina et known as reactive oxygen intermediates (ROI) or active al. 2003; Sgherri et al. 2003; Kangasjärvi et al. 2005), the oxygen species (AOS), as byproducts of metabolic pro- equilibrium between ROS generation and removal is often cesses such as respiration and photosynthesis is the price to shifted towards the former, leading to an increased produc- pay for the advantages of aerobic life. The derivatives of tion and accumulation of oxidative species. It is now clear •- molecular oxygen, including superoxide anion O2 , singlet that a common theme in the response to both biotic and abi- 1 • oxygen O2, hydroxyl radical OH and hydrogen peroxide otic stress is the generation of ROS that can be by them- H2O2 (Table 1), are in fact toxic and can damage cellular selves the primary cause of adverse effects and/or be in- constituents leading to cell death. The ability to survive volved in signal transduction pathways and changes in gene these cellular toxins depends on enzymatic and non-enzy- expression. matic detoxification mechanisms coordinately acting to re- duce cellular damage under oxidative conditions. In this ROS GENERATION AND SCAVENGING frame, Foyer and Noctor (2005) aptly described the plant cell as a network of compartments whose varying antioxi- In plant cells ROS are continuously produced as a conse- dative buffering capacities are determined by differences in quence of normal metabolism in virtually all the intracel- synthesis, transport and/or degradation of antioxidants. lular organelles, in particular in the chloroplasts, mitochon- Upon exposure to various stress conditions, such as dria and peroxisomes (Elstner 1982; Smirnoff 1993; Apel Received: 18 February, 2008. Accepted: 4 May, 2008. Invited Review Plant Stress 2 (1), 28-39 ©2008 Global Science Books Table 1 Mechanisms for the generation of Reactive Oxygen Species in must not be underestimated (Rhoads et al. 2006) and mito- 3 plant cells. Chl*, chlorophyll triplet state; Fdred, reduced ferrexoxin; chondrial ROS evolution can increase as a consequence of Fdox, oxidized ferredoxin; Fe-Sred, reduced Rieske FeS center; Fe-Sox, oxidative stress conditions that lead to ROS accumulation 2+ + oxidized Rieske FeS center; M, trace metals (Fe , Cu ); QA red, reduced in other cellular compartments thereby altering the normal quinone A; QA ox, oxidized quinone A; RH, lipid. mitochondrial function (Overmyer et al. 2003). Another •- Oxidative species Production mechanisms possible source of O2 in plants is the electron leakage to •- •- Superoxide radical (O2 ) Fdred + O2 Fdox + O2 oxygen during the monooxygenase reaction catalyzed by •- Fe-Sred + O2 Fe-Sox + O2 the cytochromes, in particular cytochrome P450, in the cyto- •- QA red + O2 QA ox + O2 plasm and the endoplasmic reticulum (Urban et al. 1997). + 2+ •- Cu + O2 Cu + O2 Finally, as will be discussed in more detail later, the •- •- + Hydrogen peroxide (H2O2) O2 + O2 + 2H H2O2 + O2 NADPH-dependent oxidase complex of plant plasma mem- Hydroxyl Radical (OH•) Haber-Weiss cycle: branes, pH-dependent cell wall peroxidases, germin-like •- n+ (n-1)+ O2 + M O2 + M oxalate oxidases, and amine oxidases have also been identi- (n-1)+ - • (n+1) M + H2O2 OH + OH + M fied as sources of ROS during biotic stress (Lamb and overall: Dixon 1997; Grant and Loake 2000; Mittler et al. 2004). •- • H2O2 + O2 OH + OH + O2 In order to control the accumulation of these toxic oxy- Fenton reaction: gen derivatives, in particular hydroxyl radicals and singlet 2+ 3+ • Fe +H2O2 Fe + OH + OH oxygen, plant cells are equipped with a battery of enzymatic 1 3 1 Singlet oxygen ( O2) Chl* + O2 O2 and non-enzymatic antioxidant systems to preserve the in- • •- + • Hydroperoxyl radical (HO2 ) O2 + H HO2 tegrity of proteins and other cellular components (Dat et al. • • • Lipid radical (R ) RH + OH R + H2O 2000; Apel and Hirt 2004). The main ROS-scavenging en- • • • Lipid peroxyl radical (ROO ) R + O2 ROO zymes and the reactions they catalyze are reported in Table • • ROO + RH ROOH + R 2. Plant cells possess several classes of superoxide dismu- 1 Lipid hydroperoxide (ROOH) RH + O2 ROOH tase (SOD) enzymes, considered the first line of defence against ROS (De Gara et al. 2003; Apel and Hirt 2004; Asada 2006). SODs are characterized by the presence of and Hirt 2004) (Fig. 1). In the chloroplast ROS are gene- diverse metal ions in their active site i.e. Cu-Zn, Mn and Fe rated in the photoreduction of oxygen to H2O2 by photo- and are located mainly in chloroplasts, mitochondria and system I electron transport (Mehler reaction), whose pri- peroxisomes as well as in the cytosol (del Río et al. 2002). mary product is superoxide anion, and in photodynamic re- The presence of SOD and of other enzymatic and non-enzy- actions occurring under conditions that limit electron trans- matic antioxidants