Reactive oxygen species as signals that modulate plant stress responses and programmed cell death

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Reactive oxygen species as

signals that modulate plant

stress responses and

programmed cell death

Tsanko S. Gechev,

1,2

* Frank Van Breusegem,

3

Julie M. Stone,

4

Iliya Denev,

2

and Christophe Laloi

1

Summary

Reactive oxygen species (ROS) are known as toxic metabolic products in plants and other aerobic organ-isms. An elaborate and highly redundant plant ROS network, composed of antioxidant enzymes, antioxidants and ROS-producing enzymes, is responsible for main-taining ROS levels under tight control. This allows ROS to serve as signaling molecules that coordinate an astonishing range of diverse plant processes. The specificity of the biological response to ROS depends on the chemical identity of ROS, intensity of the signal, sites of production, plant developmental stage, previous stresses encountered and interactions with other signal-ing molecules such as nitric oxide, lipid messengers and plant hormones. Although many components of the ROS signaling network have recently been identified, the challenge remains to understand how ROS-derived signals are integrated to eventually regulate such biolo-gical processes as plant growth, development, stress adaptation and programmed cell death. BioEssays

28:1091–1101, 2006.ß2006 Wiley Periodicals, Inc.

Introduction

ROS, resulting from excitation or incomplete reduction of molecular oxygen, are unwelcome harmful by-products of normal cellular metabolism in aerobic organisms.(1)Plants, facing an even greater burden of excess ROS, initially developed various protective mechanisms, such as small antioxidant molecules and antioxidant enzymes, to keep ROS levels under control.(2) As these protective mechanisms

became robust, plants further evolved an elaborate network of ROS-producing and detoxifying enzymes (represented by at least 289 genes inArabidopsis thaliana) to adjust ROS levels according to the cellular needs in different cell types and organs at a particular time and at different developmental stages. This evolutionary advance permitted ROS to be co-opted as signaling molecules that control cell proliferation and cell death to regulate plant growth and development, adaptation to abiotic stress factors and proper responses to pathogen attack.(3 –5)To precisely influence such diverse processes in a range of tissues at different developmental stages, the biological response to the altered ROS levels requires remarkable specificity. This specificity is ensured by multiple interacting factors, including the chemical identity of ROS, intensity of the signal, site of ROS production, developmental stage of the plant and previous stresses encountered. Interactions with other signaling molecules such as nitric oxide, lipid messengers and plant hormones are also key determinants of the final outcome of ROS signaling.(5)

Despite the obvious complexity, a clearer picture of the ROS network and its role in plant biology is slowly emerging. Recent mutational and transcriptome analyses revealed key players in the ROS network, including MAPK kinases and ROS-responsive transcription factors. In addi-tion to highlighting ROS chemistry and metabolism, this review summarizes the latest data related to plant ROS signaling. In particular, the focus is on specific factors that influence the biological processes regulated by ROS with an emphasis on plant development, stress acclimation and cell death.

1Institute of Plant Sciences, ETH Zurich, Switzerland.

2Department of Plant Physiology and Plant Molecular Biology,

University of Plovdiv, Bulgaria.

3Department of Plant Systems Biology, Flanders Interuniversity

Institute for Biotechnology, Ghent University, Belgium.

4

Department of Biochemistry and Plant Science Initiative, University of Nebraska, Lincoln, NE, USA.

Funding agencies: International Union of Biochemistry and Molecular Biology, IUBMB, grant number: S-350; The Company of Biologists Limited, EMBO, grant number: ASFTF 63.00-06; Research Fund of the Ghent University (Geconcerteerde Onderzoeksacties no. 12051403). *Correspondence to: Tsanko S. Gechev, Department of Plant Physiology and Plant Molecular Biology, University of Plovdiv, 24 Tsar Assen str, Plovdiv 4000, Bulgaria. E-mail: tsangech@pu.acad.bg DOI 10.1002/bies.20493

Published online in Wiley InterScience (www.interscience.wiley.com).

Abbreviations: ROS, reactive oxygen species; SOD, superoxide dismutase; APX, ascorbate peroxidase; GPX, glutathione peroxidase; ABA, abscisic acid.

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Chemistry of ROS

Plants, being aerobic organisms, utilize molecular dioxygen (O2) as a terminal electron acceptor. As a result of O2

reduction, highly reactive intermediates, reactive oxygen species (ROS), are produced.(1) The first step during O2

reduction leads to the formation of superoxide (O2 ) or

hydroperoxide (HO2) radicals (Fig. 1). O

2 has a short

half-life of 2 to 4ms. The second step leads to formation of hydrogen peroxide (H2O2), which is a relatively stable molecule with a

1 ms half-life. Because of this longer half-life, H2O2can migrate

from the subcellular synthesis sites to adjacent compart-ments and even neighboring cells.(6,7)The oxidizing power of O2 and H2O2 makes them potentially dangerous for the

surrounding cellular environment. O2 can inactivate impor-tant metabolic enzymes containing Fe-S clusters and alter catalytic activities.(1,2) Its protonated form, HO2, is found mainly in acidic cellular environments. HO2 can cross

biological membranes and initiate lipid oxidation by extracting protons from polyunsaturated fatty acids. In most biological systems, O2 is rapidly converted to H2O2 by the enzyme

superoxide dismutase (SOD). H2O2can inactivate enzymes

by oxidizing their thiol groups.(1)The destructive properties of

O2 and H2O2are more prominent when they interact in the

presence of metal ions to form the highly reactive hydroxyl radical (HO) during the so-called Haber-Weiss reaction.(8) HOcan react with and damage virtually anything with which it comes into contact.(1)Because HOis highly reactive, cells do not possess enzymatic mechanisms for HO detoxification and rely on mechanisms that prevent its formation. These mechanisms include the preceding elimination of O2 and H2O2and/or sequestering metal ions that catalyze the

Haber-Weiss reaction with metal-binding proteins, such as ferritins or metallothioneins.(9,10)

Singlet oxygen (1O2) is a non-radical ROS produced by spin

reversal of one electron of the ground state triplet oxygen (3O2).(11)Such spin reversals occur under input of energy and

are most often caused by reaction with the highly energized triplet-state chlorophyll.(11)If not quenched by carotenoids, 1O

2can in turn transfer its energy to other molecules and

damage them, like the rapid peroxidation of polyunsaturated fatty acids.(1)

An important feature of ROS chemistry is the conversion of one ROS into another. In addition to reacting with H2O2and

forming HO, O2 can react with nitric oxide radical (NO) to form peroxynitrite (ONOO). Peroxynitrite is rapidly proto-nated to peroxynitrous acid (ONOOH), which is a powerful oxidizing agent. It can damage all biomolecules and initiate reactions leading to formation of several other destructive radical- and non-radical reactive species.(1)

ROS homeostasis

Sites and sources of ROS production

The multiple sites and sources of ROS production increase the complexity of ROS. ROS are normal products of metabolism and are produced in all cellular compartments within a variety of processes (Fig. 2).(4) In general, they are maintained at constant basal levels in healthy cells, but their levels transiently or persistently increase under different stress conditions or in response to developmental signals.

Chloroplasts are a major site of ROS generation in plants.(12) Photosynthetic electron transfer chains produce O2 , especially under conditions leading to overenergization of

the electron transfer chains.(4) O

2 is formed mainly by

electron leakage from Fe-S centers of photosystem I or reduced ferredoxin to O2(Mehler reaction), which is then

quickly metabolized to H2O2 by SOD. Although excessive

production of ROS is dangerous, in this case the ability of oxygen to accept electrons prevents overreduction of the electron transport chains, thus minimizing the chance of1O2

production.(4) 1O2is produced by energy transfer to3O2from

the excited triplet state chlorophyll in photosystem II, especially under high light intensities.(11) Carotenoids can quench1O2directly, a role that is shared with tocopherols, or

prevent1O2formation by quenching the excited triplet state

chlorophyll.(12)

Peroxisomes and glyoxysomes are other major sites of ROS generation during photorespiration and fatty acid oxidation, respectively.(13) Photorespiration is a complex

process tightly linked to photosynthesis. Under conditions that impair CO2fixation in chloroplasts, the oxygenase activity of

ribulose-1,5-bisphosphate carboxylase/oxygenase increases and the produced glycolate moves to peroxisomes, where it is oxidized by glycolate oxidase forming H2O2. Fatty acid

oxidation in glyoxysomes of germinating seeds generates H2O2 as a by-product of the enzyme acyl-CoA-oxidase.

Mitochondrial respiration is another process leading to O2 and H2O2formation.(14)The main sources of ROS production

in mitochondria are NADH dehydrogenase, ubiquinone radical and complex III.(14)Although mitochondrial ROS production is much lower compared to chloroplasts (lack of light energy-absorbing chlorophyll pigments), mitochondrial ROS are important regulators of a number of cellular processes, including stress adaptation and programmed cell death.(15) The estimated H2O2production in mitochondria may be 20

times lower than in the chloroplasts, at least in C3plants.(16) Figure 1. Production of ROS by multistep reduction of

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Plasmalemma-bound NAD(P)H oxidases as well as cell-wall-associated peroxidases are the main O2 and H2O2

producing apoplastic enzymes.(17) These are regulated by various developmental and environmental stimuli.(4) Apoplas-tic ROS accumulation parApoplas-ticipates in the so-called oxidative burst observed as a part of the hypersensitive response to pathogens but also regulates cell growth, development and cell death.(3,5,17 –19) O

2 and H2O2 are produced also by

xanthine oxidase during purine catabolism, ribonucleotide reductase during deoxyribonucleotide synthesis and various other oxidases induced by biotic and abiotic stresses.(4)

ROS detoxification

A strict control of ROS levels is essential to prevent their toxicity and to ensure an accurate execution of their signaling functions. Therefore, plants have evolved an elaborate enzymatic and non-enzymatic antioxidant system, which together with the ROS-producing enzymes maintains ROS homeostasis in all cellular compartments and regulates the adjustment of ROS levels according to the cellular need at a particular time (Table 1).(10)SODs are the only plant enzymes capable of scavenging

O2 , whereas H2O2can be catabolized directly by catalases or

with the help of various reductants by ascorbate peroxidases

Figure 2. Schematic representation of a generalized plant cell depicting major sources of ROS generation and scavenging enzymes described in the text. Much of the ROS generated in photosynthetic plant cells is produced in chloroplasts. Chloroplasts produce singlet oxygen (1O2) from the excited triplet state chlorophyll (primary source Photosystem II, PSII) and superoxide anion (O2 ) in the Mehler reaction (primary source PSI). Mitochondria produce O2 due to electron leakage from the mitochondrial electron transport chain. O2 from both organelles is then rapidly converted to hydrogen peroxide (H2O2) by superoxide dismutases (SOD). H2O2, in turn, is detoxified by

ascorbate peroxidases (APX) with the ascorbate (AsA) as an electron donor. AsA, oxidized to monodehydroascorbate radical (MDA) and eventually to dehydroascorbate (DHA), is then recycled in the Halliwell-Asada pathway(4)via a series of enzymatic reactions involving monodehydroascorbate reductase (MDHAR), reduced ferredoxin (Fd), dehydroascorbate reductase (DHAR), glutathione reductase (GR) and non-enzymatic antioxidant glutathione (reduced form GSH, oxidized form GSSG). Peroxisomes and glyoxysomes produce large amounts of H2O2during photorespiration and fatty acid oxidation, respectively. This H2O2is rapidly scavenged by catalases (CAT). Plasma

membrane-bound NADPH oxidases generate superoxide anion in the apoplast, which then dismutates to H2O2. The movement of H2O2

between different cellular compartments is facilitated by peroxoporins (specialized aquaporins). The excess H2O2leaking into cytosol from

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(APX), peroxiredoxins, glutathione peroxidases (GPX) and the heterogenous group of guaiacol peroxidases.(4) Nonenzy-matic antioxidants also contribute to ROS homeostasis, with ascorbate, glutathione, tocopherol and carotenoids as the most-abundant water- and lipid-soluble antioxidants.(20)

As catalase degrades H2O2without any reducing power,

this enzyme provides plants with an energy-efficient way to remove H2O2. However, catalase is active only at relatively

high H2O2concentrations. Lower H2O2levels are eliminated

by APX and other peroxidases with the aid of various reductants like ascorbate and glutathione. While some of the ROS network enzymes as SOD, catalase and APX are entirely dedicated to ROS homeostasis, others like guaiacol

perox-idases, thioredoxins, ferritins and glutathione-S-transferases are involved also in other processes related to control of development, redox regulation of target proteins and detox-ification reactions (Table 1). Some of the ROS-associated enzymes, like guaiacol peroxidases, thioredoxins, glutaredox-ins and glutathione-S-transferases, have evolved into large multigene families with diverse functions that facilitate the adaptation of photosynthetic organisms to terrestrial life in elevated oxygen concentrations and different stressful envir-onments.(21– 25) These and other antioxidant enzymes

to-gether with the ROS-producing enzymes constitute a highly sophisticated and redundant network, which inArabidopsis thalianaconsists of at least 289 genes (Table 1).

Table I. Major plant ROS-associated enzymes and antioxidants

Enzyme/antioxidant (in brackets: number of

genes inA. thaliana) Function Localization Reference

Superoxide dismutases (SOD) (8) Dismutation ofO2, leads toH2O2formation cyt, chl, mit, per (10)

Catalases (3) DetoxifiesH2O2; no reductor required mit, per, gly (4)

Ascorbate peroxidases (APX) (9) DetoxifiesH2O2withascorbateas reductor cyt, chl, mit, per, (12)

Monodehydroascorbate reductases (MDHAR) (5)

Reducesmonodehydroascorbate radicalswith NAD(P)H as reductor

cyt, chl, mit (10) Dehydroascorbate reductases

(DHAR) (5)

Reduces dehydroascorbate radicals with GSH as reductor cyt, chl, mit (10) Glutathione reductases (GR) (2) Reducesoxidized glutathionewith NADPH as reductor cyt, chl, mit, per (10) Guaiacol peroxidases (POX) (73) DetoxifiesH2O2with various substrates as reductors; can also

produce ROS (O2,HO,HOO). Involved in lignin

biosynthesis, hormone metabolism, cross-linking of cell wall polymers, pathogen defense, plant development, senescence and symbiotic interactions

cw, cyt, mit, vac (21, 24)

Glutathione peroxidases (GPX) (8) DetoxifiesH2O2andlipid hydroperoxideswithGSHas reductor cyt, chl, mit, er (10)

Glutathione-S-transferases (GST) (53)

Detoxification reactions (Degluthathionylation). Can detoxifylipid hydroperoxidesand exhibitDHAR activity. Can act as non-catalythic cariers that facilitate the distribution and transport of various biomolecules

apo, cyt, chl, mit, nuc (25)

Peroxiredoxins (Prx) (10) Thiol-containing peroxidases, detoxifyH2O2 cyt, chl, mit, nuc (10)

Thioredoxins (Trx) (46) Redox-control of enzymes and transcription factors, electron donor to

PrxandGPX

cyt, chl, mit, nuc (22) Glutaredoxins (Grx) (31) Deglutathionilation, redox-control of enzymes and transcription

factors, electron donor toDHAandPrx. Protection against oxidative damage, regulation of plant development.

plasmalemma,cyt, chl, mit, er

(23) Ferritins (4) Bindsiron, thus sequestering it in a bioavailable, non toxic form and

preventing formation ofHO. Iron homeostasis

chl, mit (9) Alternative oxidases (AOX) (6) Channels electrons from electron transfer chains of mitochondria and

chloroplasts directly to oxygen, thus minimizingO2production

under conditions that favour electron transport chain over energization. The chloroplastic AOX homologue Immutans participates also incarotenoidbiosynthesis

chl, mit (10)

Ascorbate Substrate forAPX. DetoxifiesH2O2 apo, cyt, chl, mit, per, vac (12)

Glutathione Substrate for various peroxidases, glutathione transferases and glutathione reductases. DetoxifiesH2O2, other hydroperoxides

and toxic compounds

apo, cyt, chl, mit, per, vac (4)

a-Tocopherol Protects membrane lipids from peroxidation, detoxifies

lipid peroxidesand quenches1O 2

membranes (20) Carotenoids Quench1O

2. Photosystem assembly, key components of the light

harvesting complex, precursors of ABA

chl, chromoplasts, elaioplasts, amyloplasts

(20) Flavonoids Can scavengeH2O2andHOdirectly. vac (26)

The abbreviations are: cw, cell wall; apo, apoplast; cyt, cytosol; chl, chloroplasts; mit, mitochondria; er, endoplasmatic reticulum; vac, vacuole; per, peroxisomes; gly, glyoxysomes; nuc, nucleus

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All cellular compartments are well-equipped with antiox-idant enzymes and antioxantiox-idants (Fig. 2, Table 1). Therefore, ROS are normally scavenged immediately at the sites of their production by the locally present antioxidants. However, when this local antioxidant capacity cannot cope with ROS produc-tion (for example, during stress or temporarily reduced antioxidant levels due to developmental signals), H2O2can

leak into the cytosol and diffuse to other compartments. Plants can also deal with excess H2O2by transporting it into vacuoles

for detoxification.(7,26) Vacuoles are very rich in flavonoids,

powerful antioxidants that can scavenge various ROS and peroxynitrite.(27)They also contain high levels of ascorbate, glutathione and peroxidases localized at the tonoplast inner surface.(26)

ROS signaling

How is ROS specificity ensured?

ROS are not just toxic products that need to be eliminated. Spatial and temporal fluctuations of ROS levels are interpreted as signals required for growth, development, tolerance to abiotic stress factors, proper response to pathogens and cell death (Fig. 3).(5,18,28 – 30) It is of principal importance to

understand how such simple molecules can regulate so many diverse processes in different cell types and organs, and at different developmental stages. It has become increasingly clear that the specificity of the biological response to the altered ROS levels depends on multiple factors: chemical identity of the ROS, intensity of the signal (dose-dependent effect), sites of production, developmental stage of the plant, pre-history of the plant cell (for example, previous stress encounters), and interaction with other signaling molecules such as nitric oxide, lipid messengers and plant hor-mones.(31,32)

Most ROS seem to possess signaling functions that enable them to regulate specific biological processes. Initially, signaling functions were attributed to H2O2and

comprehen-sive transcriptional analysis by microarray- or AFLP-based technologies identified H2O2-responsive genes.(33 –38) Later,

signaling properties and distinct transcriptional responses were confirmed for the other ROS.(39– 41)A recent comparative meta-analysis of microarray datasets obtained from plants accumulating different ROS at different subcellular locations revealed specific transcriptomic footprints for O2 , 1O2and

H2O2.(42)

The biological outcome of ROS signaling is intrinsically related to the nature of the ROS signal and is exquisitely dose dependent.(39,40,43)Low doses of O2 and H2O2have

been shown to induce protective mechanisms and acclimation responses against oxidative and abiotic stress, while high doses trigger cell death.(39,43)Interestingly, cell death initiated by high doses of H2O2and1O2can be uncoupled from the

necrosis caused by even higher doses of these ROS.(11,44,45)

How specificity in plant cells is transduced is unclear but it could be due to activation of different MAP kinases and transcription factors, as it is proposed for Schizosaccharo-myces pombe.(46)

Aside from the type, dose and duration of ROS signal, the site of ROS production is also a critical determinant.(27,47)For example, localized production of O2 by NADPH oxidase in the root hair tip triggers Ca2þpeaks necessary for the root hair growth.(18)This spatial regulation of NADPH oxidase activity is regulated by the Rho-like GTPases.(28)These GTPases also control tracheary elements differentiation through localized ROS production.(48) The issue of spatial control of ROS production is tightly linked with the aspect of ROS mobility and communication between different cellular compartments. While 1O

2, O2 and especially HO

are not very mobile,

Figure 3. Plant processes regulated by ROS. Developmental processes, stress responses and biotic interactions regulated by ROS include root growth, elongation and gravitropism, stress tolerance and systemic acquired acclimation (SAA), tracheary elements development (TE), senescence, hypersen-sitive response (HR) to pathogens, systemic acquired resis-tance (SAR) and plant–plant allelopathic interactions.(3,18,86,91)

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H2O2 can migrate quite a distance from the site of its

production and cross biological membranes.(7) However, membranes are not very permeable for H2O2and the transport

is most likely carried through specialized aquaporins called peroxoporins.(6,7)This transport is another way of adjusting local concentrations, thus the biological effect of H2O2. An

example of cross-compartment communication associated with H2O2mobility is the increased levels of H2O2produced in

cytosol in the absence of the cytosolic APX, which leads to inhibition of chloroplastic APX and collapse of the chloroplastic antioxidant system.(49) Also peroxisomal catalase can act as a sink for H2O2 produced in peroxisomes or elsewhere

and catalase infiltrated in the extracellular space of leaves can scavenge photorespiratory H2O2 produced in

peroxi-somes.(50)

ROS and other signaling molecules

Interaction with other signaling molecules such as nitric oxide (NO), lipid messengers or plant hormones determine the outcome or help to fine-tune the biological responses to altered ROS levels.(31,32) NO interacts with O

2 and H2O2 in a

complex manner to regulate cell death during the hypersensi-tive response.(51) It has been proposed that ROS are key

mediators in channeling NOinto the death pathway. Indeed, Arabidopsis thaliana overexpressing the H2O2-detoxifying

enzyme thylakoid APX showed increased resistance towards NO-induced cell death.(52) Recent transcriptome analyses identified genes commonly regulated by NOand H2O2as well

as genes that are specifically responsive to the two stress signals in tobacco.(53)

Several lipid-derived messengers that interplay with ROS have been described. ROS, in particular HO, can initiate nonenzymatic formation of hydroperoxy fatty acids and other oxidized lipids collectively known as oxylipins.(54) Phytopros-tanes are a major group of prostaglandin- and jasmonate-like oxylipins that are constantly produced in healthy cells, but their levels increase under various stresses.(54,55)Phytoprostane

B1, for example, can trigger detoxification and defense res-ponses, and plants primed with phytoprostane B1 become more tolerant to oxidative stress-induced cell death.(55) Sphingolipids are other biologically active lipids that regulate plant growth and cell death.(58) Disruption of sphingolipid metabolism by the fungal AAL-toxin in AAL-toxin-sensitive plants leads to H2O2 accumulation and subsequent cell

death.(57)The link between sphingolipid and redox signaling is further substantiated by isolating mutants altered to fungal toxin- and ROS-induced cell death(30)(T. Gechev, M. Ferwerda, L. Bernier, J. Hille, unpublished results). Phospholipids are other bioactive molecules that can modulate ROS res-ponse.(58)These second messengers are rapidly formed in response to a variety of stimuli via the activation of lipid kinases or phospholipases. For example, the oleate-stimulated

phos-pholipase D and phosphatidic acid can inhibit H2O2-induced

cell death inArabidopsis thaliana.(59)

Interaction of ROS with plant hormones can be another determinant of specificity. For example, auxin, abscisic acid (ABA) and jasmonic acid together with ROS regulate such diverse processes as growth, stomatal closure and wounding responses.(32) Likewise, ethylene and salicylic acid act synergistically with ROS.(60) Increased synthesis of both

ethylene and salicylic acid is observed under abiotic stress and pathogen attack, which can in turn potentiate ROS production.(60)Recent evidence implicate complex ethylene interactions with ABA and H2O2 to regulate stomatal

closure.(61) Next to the interactions with the classical hor-mones, a number of polypeptides, including systemin and the recently identified polypeptide AtPep1, can induce H2O2

synthesis and activate defense gene expression inArabidopsis thaliana.(62,63) The AtPep1 induces also its own precursor genepropep1, suggesting a possible amplification of the ROS signal.(63)Indeed,propep1and one of its paralogs are highly induced in a number of stresses leading to H2O2

accumula-tion.(57,63)

Perception and transduction of ROS-derived signals

While specific ROS sensors in plants remain elusive, there is ample data pointing out different components of the ROS signaling network, including kinases, phosphatases and ROS-responsive transcription factors.

The conditional fluorescent (flu) mutant accumulates free protochlorophyllide in darkness.(64) Upon re-illumination, the excited protochlorophyllide acts as a photosensitizer and generates1O2. Theflusystem seems to be very specific in

generating only1O2and not O2 or H2O2.(40) 1O2, produced in

the chloroplasts, generates a signal that migrates to the nucleus where it switches on genetic programs leading to growth inhibition or/and programmed cell death.(11) The

chloroplastic protein EXECUTOR1 is probably situated at the beginning of the1O

2signaling cascade asexe1 fluplants

show no growth inhibition or cell death upon dark to light shift.(65)

The zinc finger proteins LSD1 and LOL1 are negative and positive regulators, respectively, of O2 - induced cell death in Arabidopsis thaliana.(66,67)It has been proposed that they act together as a molecular rheostat to sense and transmit the O2 -derived signal. The phenotype oflsd1mutant is

uncon-trolled, spreading cell death, initiated by O2 . (68)

Interestingly, a triple mutant betweenlsd1and two ROS-generating NADPH oxidase homologues,atrbohDandatrbohF, showed uncon-trolled cell death even under growth conditions that normally represslsd1cell death.(29)Thelsd1phenotype was restored by overexpression of AtrbohD, demonstrating that O2

produced by NADPH oxidase and its subsequent dismutation to H2O2is somehow able to antagonize the O2 -induced cell

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death in the neighboring cells.(29) In accordance with that observation, catalase overproducing tobacco plants with reduced levels of H2O2have larger hypersensitive response

lesions upon challenge with tobacco mosaic virus.(69)A similar antagonistic effect has been observed between1O2and H2O2.

Overexpression of the H2O2-scavenging enzyme

thylakoid-bound APX in flu increases further 1O2-dependent growth

inhibition and cell death (C. Laloi and K. Apel, unpublished results), indicating that some of the H2O2-regulated genes

may negatively control1O

2signaling.

Mitogen-activated protein kinases (MAPK) are widespread signal transmitters in eukaryotes. InArabidopsis thaliana, a multifaceted network of kinases is involved in relaying the H2O2

signal. ANP1, a MAPK kinase kinase, is activated by H2O2

and, through an unidentified intermediate kinase, in turn activates two downstream MAPKs, AtMPK3 and AtMPK6, which eventually upregulateGST6 andHSP18.2genes.(70) Overexpression of ANP1 in transgenic plants resulted in increased tolerance to heat shock, freezing and salt stress.(70) The serine/threonine kinase OXI1 (oxidative signal-induci-ble1) is another essential component of the H2O2signaling

network in Arabidopsis thaliana. The oxi1-null mutant has abnormal root hair growth and enhanced susceptibility to pathogen infection, two processes mediated by H2O2.(71)OXI1

is activated by H2O2and abiotic stresses and OXI1 is needed

for full activation of AtMPK3 and AtMPK6.(71)Another H2O2

-inducible kinase is OMTK1 (oxidative stress-activated MAP triple-kinase 1) in alfalfa.(72)In contrast to OXI1, OMTK1 is H2O2 specific and not activated by abiotic stresses or

hormones. OMTK1 activates the downstream MAP kinase MMK3. MMK3 can also be activated by ethylene and elicitors, thus serving as a convergence point of ethylene and ROS signaling.(72)H2O2also increases expression of theArabidopsis

thaliana nucleotide diphosphate kinase 2 (AtNDPK2).(73) AtNDPK2 overexpression reduced the accumulation of H2O2

and, like ANP1, resulted in enhanced tolerance to cold, salt and oxidative stress.(73)It has been shown thatArabidopsis

thaliananucleotide diphosphate kinase 1 (AtNDK1) interacts with the threeArabidopsis thalianacatalases in a yeast two-hybrid system and transgenic plants overexpressing AtNDK1 exhibited resistance to paraquat and enhanced ability to detoxify H2O2.

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Protein phosphatases, which are equally as important for modulating the signal, have also been implicated in ROS signaling recently.(75)

One of the earliest events that follow elevation in H2O2

levels is alteration in calcium ion fluxes.(71,76)Transient Ca2þ oscillations are specific for different types of stress and can lead to various downstream effects through the numerous Ca2þ-interacting proteins, including calmodulins and calcium-dependent protein kinases that are involved in different, sometimes even antagonistic responses.(76)While some of them, like NAD kinase, aid in the production of H2O2 by

generating more substrate for NADPH oxidase, others like

catalase have the opposite effect.(77) Effects mediated by Ca2þcan be rapid and short-term, as with the activation of calcium channels by hydrogen peroxide following abscisic acid signaling in guard cells, (78) or long-term, which relies on altered gene expression.

Activation of MAPK cascades, alterations in Ca2þfluxes and other biochemical changes associated with the relay of ROS signals ultimately lead to activation of ROS-sensitive transcription factors. Genetic and molecular data identified transcription factors that rapidly respond to different ROS.(33,36 – 38,40,57) A recent comparative analysis of tran-scriptome changes induced by different types of ROS in Arabidopsis thaliana identified transcription factors that are specifically responding to each of the different ROS as well as others that are induced by all types of ROS.(42)While several members of the ERF and Myb family transcription factors are specifically induced by1O2, the heat-shock regulon seems to

specifically respond to H2O2.(33,42)Heat-shock transcription

factors have been proposed as possible H2O2sensors and the

downstream genes are involved not only in heat-shock tolerance but play more general roles in defense against variety of stresses, including oxidative stress.(79)The induction

ofArabidopsis thaliana Apx1gene whose promoter contains heat-shock-factor-binding motif substantiates these find-ings.(80) Two genes encoding WRKY-family transcription factors and two zinc-finger transcription factors ZAT11 and ZAT12 were commonly upregulated by O2 ,1O2and H2O2.

ZAT12 has been attributed an important role in abiotic stress signaling as ZAT12 overexpressors have elevated transcript levels of oxidative- and light stress-responsive transcripts and ZAT12-deficient plants are more sensitive to H2O2-induced

oxidative stress.(80,81)

Processes regulated by ROS Plant growth and development

ROS are involved in the regulation of several developmental processes, including root hair growth and elongation, apical dominance, leaf shape, tracheary elements maturation, trichome development, aleurone cell death and senescence (Fig. 3). The function ofArabidopsis thalianaNADPH oxidases was initially thought to be ROS production during the hypersensitive response and supported with genetic data demonstrating decreased ROS accumulation after pathogen challenge in a double mutant of two NADPH oxidase homologuesatrbohDandatrbohF.(19)However, theatrbohD atrbohFdouble mutant also has reduced ABA-mediated seed germination and root elongation inhibition.(82) Further evi-dence for the role of ROS in growth and development came from the studies on theatrbohCmutant which has low ROS levels in root hairs and is defective in activation of Ca2þ channels required for formation of Ca2þgradient necessary for

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Arabidopsis thaliana oxi1-null mutant has reduced root hair growth.(71)In contrast, H2O2production may have an inhibitory

effect on growth, as suggested by the inhibition of auxin responses by ANP1, the MAPK kinase kinase that relays H2O2

signal inArabidopsis thaliana.(70)Indeed, many auxin-respon-sive genes are downregulated in response to elevated H2O2

levels.(33,57)

Cell death

Cell death is essential for plant growth, development and proper responses to the environment.(45)At the same time, cell death can be an unwanted event during many unfavorable environmental conditions, including heat, cold, salt and xenobiotic stresses and compatible or disease-causing plant–pathogen interactions.(83,84)Developmental or environ-mental cell death controlled by ROS occurs during the aleurone cell death, leaf senescence, a number of abiotic stresses, the hypersensitive response and allelopathic plant– plant interactions.(30,85,86) Programmed cell death can be initiated by all types of ROS.(39,40,87) In addition, hydroxyl radical-initiated lipid peroxidation is a rich source of oxidized lipids that can trigger programmed cell death on their own or in concert with other ROS.(44,54)Two well-described instances of

ROS-induced programmed cell death in development are organ senescence and aleurone cell death. ROS, together with ethylene, are hypothesized to regulate plant organ senescence through peroxisomal and chloroplast-derived signals.(88,89) During seed germination, monocot aleurone layer cells utilize their carbohydrate reserves by gibberellic acid-dependent synthesis of alpha-amylase, rapidly followed by cell death.(90)This cell death is dependent on glyoxysomal production of H2O2 during the utilization of lipid reserves.

There is evidence that glyoxysomal antioxidant enzymes catalase, ascorbate peroxidase and superoxide dismutase are downregulated by gibberellic acid to ensure sufficient accu-mulation of H2O2prior to the onset of cell death.(90)

One of the best-studied types of cell death is the hypersensitive response to pathogens.(30)During the

hyper-sensitive response, a biphasic burst of NADPH-dependent ROS production is an essential component for the onset of local cell death in the proximity of the infection as well as for the initiation of signal that migrates in the neighboring tissues to trigger distant micro-hypersensitive response and induce systemic acquired resistance.(91) Although, in the case of many plant–pathogen interactions, programmed cell death is a welcome event for the plant host, there are examples of pathogen-triggered cell death that are detrimental for the plant. Several necrotrophic fungal pathogens produce myco-toxins that are able to induce ROS accumulation and eventually programmed cell death, using this strategy as a method to kill the plant and feed on the dead tissue.(57,92)

In addition to plant–pathogen interactions, a role for programmed cell death in allelopathic plant–plant interactions

have been described recently.(86) Centaurea maculosa roots secrete the phytotoxin catechin, which triggers ROS accumulation in root meristems of neighboring species and subsequent Ca2þ- dependent cell death. In this way, Centaurea maculosakills and eventually displaces other plant species from their habitat.

Stress acclimation

ROS have emerged as important regulators of plant stress responses. Many unfavorable environmental condi-tions lead to oxidative stress due to increased ROS production or/and impaired ROS detoxification.(4,10) Accumulation of ROS is observed during cold, heat, drought, high-light, heavy-metal stress and exposure to fungal toxins.(4,57) In addition, H2O2is a secondary messenger during wounding

responses and various biotic interactions.(62,86) Redox changes are sensed by the plant cell as a ‘warning’ message and, depending on the situation, genetic programs leading to stress acclimation or programmed cell death are switched on.(43)

Transient and a moderate elevation of ROS result in protection against subsequent more severe abiotic or oxidative stress. This stress acclimation can be induced either by a direct application of ROS or ROS-generating agents, or by application of mild sublethal stresses that lead to transient ROS accumulation. One of the first studies on stress acclimation demonstrated that a H2O2pretreatment of maize

seedlings protected them from chilling stress.(93)This protec-tive effect resembled the effect of a pretreatment with ABA and low temperatures. Indeed, H2O2 was found to accumulate

during the ABA- and low temperature-acclimation treat-ments.(93) H2O2 pretreatments have been shown to also

induce salt, high-light, heat and oxidative stress toler-ance.(43,94,95) Amazingly, H2O2-induced acclimation to high

temperature is very durable, lasting more than a month after the initial H2O2 treatment.(95) Applications of salicylic acid,

causing elevation of H2O2levels, or low doses of the O2

-generating herbicide paraquat protect against subsequent severe heat or oxidative stress, respectively.(39,96) In both

mustard and potato, heat acclimation treatment elevates H2O2

levels and results in subsequent thermotolerance against severe heat shock, which is consistent with the thermopro-tective role of H2O2treatment.

(95,96)

Likewise, light acclimation and H2O2pretreatment can result in tolerance against high

light stress.(94)Moreover, it has been proposed that H2O2can

initiate acclimation not only in local leaves but also in distant non-acclimated leaves, a process referred to as systemic acquired acclimation.(94)ROS are also the signal messengers that initiate cell death-protective responses in the neighboring cells that surround the sites of the hypersensitive response to pathogens and trigger systemic acquired resistance in distant tissues.(29,91)In this context, it is not surprising to find that

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manipulation of ROS levels can alter the resistance to pathogen attack.(97)

The stress tolerance achieved by transient elevations in ROS levels can be explained by preactivation of defense mechanisms, including kinases, transcription factors and other components of the signaling network, antioxidant enzymes, dehydrins, low-temperature-induced, heat-shock and pathogenesis-related proteins.(39,43,73,94)H

2O2

pretreat-ments of maize and tobacco that resulted in induced protection against chilling, light and oxidative stress increased the activities of the catalase, ascorbate peroxidase, guaiacol peroxidases and elevated the levels of GPX protein.(43,93) Tobacco plants with reduced catalase activity have elevated levels of pathogenesis-related proteins and enhanced resis-tance against pathogens.(97) A number of transcriptome surveys supported these initial observations and identified new batteries of genes highly regulated at the transcriptional level during ROS-induced stress acclimation.(39,98)The newly identified genes implicated in the acclimation process included putative components of signaling cascades (kinases, phos-phatases, Ca2þ-interacting proteins), transcription factors that presumably govern the global transcriptional re-programming during acclimation and other genes, most of them representing functions that directly or indirectly ensure stress protec-tion.(39,98)Subsequent functional studies confirmed the role of some of those genes in stress tolerance and acclima-tion.(73,80,81)

Both sets of genes that participate in stress acclimation induction and genes responsible for the maintenance of systemic acquired acclimation are important for durable acclimation. The heat-shock protein HSA32, for example, is required not for induction but for maintenance of acquired thermotolerance, as demonstrated by the inability of knockout hsa32 plants to survive severe heat shock followed by a recovery period longer than 24 hours.(99)

Multiple stresses exist in nature and different stressors may require diverse responses and adjustment of multiple adapta-tion mechanisms.(100)Manipulating ROS levels provides us

with an opportunity to enhance specific and common protective mechanisms against different stresses to ensure plant growth and survival under a variety of unfavorable environmental conditions.

Conclusions

It is becoming increasingly evident that ROS regulate a complex signal transduction network within the plant develop-ment and its response and adaptation to both biotic and abiotic stressors. We highlighted the major sources of ROS and sites of production in plant cells, together with the key antioxidant molecules and enzymes that scavenge ROS. To effectively function as signaling molecules, a fine-tuned balance of ROS production, conversions and metabolism needs to be main-tained in all cellular compartments, cell types and organs

during different developmental stages. Perturbations of this balance in any direction have profound effects on plant growth or survival. Therefore, a highly sophisticated and flexible system of small molecules, proteins and lipids are responsible for controlling ROS homeostasis. These days, ROS-respon-sive genes and their transcriptional regulators together with ROS-directed regulatory mechanisms and target molecules are being discovered on a regular basis. Although a clearer picture of the interplay between ROS and signal transduction components is beginning to emerge, the challenge remains to integrate these new players into the ROS signaling network. Continued high-throughput functional genomics efforts and other emerging technologies will foster additional insights that will provide a more detailed picture of the networks involved in different ROS-related plant processes. These new insights will also allow the identification of new candidate genes that can ultimately be exploited to modulate ROS-related plant processes that lead to the generation of better performing crops.

Acknowledgments

Authors wish to thank Viktor Ivanov for artwork.

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