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This article isprotected bycopyrig 10.1111/nph.15488 doi: lead todifferences version between this andthe ofPleasecite ar Version Record. this been and throughtypesetting, proofreadingwhich may thecopyediting, process, pagination AcceptedThis Contents Accepted: 28 August 2018 Received: 10 April 2018 0000 ArticleCorresponding author: Biosciences, College Nicholas Smirnoff and DominiqueArnaud Hydrogen peroxide metabolism Articletype : NICHOLASPROF. SMIRNOFF (Orcid ID : 0000 VIII. VII. VI. V. IV. III. II. I. Summary

-

article undergone hasfor and b accepted been review publication fullpeer

0001

- Hydrogen peroxidesignalling Metabolicfunctions hydrogenof peroxide Control of hydrogen peroxideconcentration: howand where? Hydrogen peroxidetransport Production of Hydrogen peroxideand superoxide toxicity Measuring and imaging hydrogen peroxide Introduction 5630

- Commissioned Material 5602 of Lifeof and Environmental Sciences, University of Exeter, ExeterEX4 4QD, UK.

Nicholas Smirnoff

hydrogen peroxide: enzymesand subcellular locations

ht. All rightsht. All reserved.

-

[email protected]

and functions Tansley Review - 0001 - 5630

- 5602)

in in plants

. +44 725168, (0)1392

ut hasnot ORCID: ORCID: ticle as provided byOpenResearchExeter brought toyouby

CORE This article isprotected bycopyrig been extensively reviewed. This reviewis distinct in attempting to assess knowledgeour H of (H In recent years considerableattention hasbeen paid to the involvement I. peroxiredoxin, hydrogen peroxide Ke signalling roles. combined with detection of specificproteins modifiedH by resolution geneticallyof Quantification of the sourcesand sinks H of thiol pr signal transduction mechanisms arepoorly example during acclimation stress to and pathogen defence, hasreceived much attention butthe chloroplastand peroxisomeautophagy and pr lignification and, possibly, cell development and defence involvementby its in typeIII peroxidase all of which havecell compartment removed by catalase,peroxiredoxin, glutathioneperoxidase and other apoplastic and mitochondria, plasma membraneNADPH oxidases, peroxisomal oxidases, typeIII peroxidases H Summary 2 Introduction oteins oteins to the sulfenicacid form and, similarly to otherorganisms, this modification could initiate 2 O ywords:

AcceptedO Article IX. 2 References Acknowledgements - 2

is produced, based redox relays andtarget modify enzymes, receptor kinasesand transcription factors. )

and reactive associated oxygen species in(ROS) plantfunction. Consequently,the topic has

oxidative stress, peroxidase,reactive oxygen species Where next?Where

via oxidases. Intracellular transportis facilitated by aquaporins and H superoxideand superoxidedismutase, by electron transportin chloroplasts

- encoded H expansion

( - H 2 specific isoforms. Apoplastic H O 2 ht. All rightsht. All reserved. O 2 sensors such as HyPerand roGFP2 2 )

, ascorbate peroxidase via - 2 defined. H O H 2 ogrammed cell death. The roleof H 2 O is being im 2 - derived hydroxyl radicals. Excess H 2 O 2

oxidises specific oxidises cysteine residues of target proved by thespatial and temporal 2 - O like enzymes and ascorbateperoxidase,

2

will allowdeeper understanding its of

(APX). (ROS) 2 - O mediated polymercross 2

, superoxide,catalase,

influences ce

of hydrogenof peroxide - Orp1. These H 2 O ll expansion, 2

2 in signalling, for O 2 2 O

2 triggers 2 O

is 2 - sensors linking, 2 O 2

This article isprotected bycopyrig activity to providefast reaction rates,and isDAB notsuitable for livecell imaging.use The of these Amplex Red and (3,3’DAB al.et reactivespecies (RS), including peroxinitrite dichlorodihydrofluorescein diacetate(CM dichlorodihydrofluorescein diacetate( Noctor quantifying imaging or H reagentssuch as AmplexDAB, Red and fluorescein pragmatic responseto a lackof practical alternatives. All commonly usedfluorescent colouredor methods are often applied without critical evaluation sufficientor controls. This si temporal resolution ROS havebeen extensively criticised for their lack chemicalof specificity and insufficient spatial and and spatial resolution Critical to understan II. metabolism and signalling (Sections VII and VIII). production, transportand removal of peroxide (Sections IV H of potentially signals that affectprotein modifications of cellular components. These modifications include oxidative damagebut are also production andarray the of consequences that arisein terms radicalof production and specificitycomplicated is by “downstream” radical formation. reactions nitric of oxide(NO H beused as a substrate and signalling moleculein a relatively controllable manner. Superoxide and relatively stablein biological systems compared to its usual precursor superoxide (O methods focuswith a genetically on consequently understandingour hampered. is Therefore we critically assessH physiological processes. This situationcaused is by the difficulty in measuring specificROS and (Fig.but a 1) largeproportion of possible H on function inthecontext itsof metabol 2 O

AcceptedMeasuringand imaging hydrogen peroxide Article 2 2

O , 2016) producti 2

et al. the review will coverpotential targets of H . A useful critical assessment CMof , 2016) 2 on areon therefore entangled, a situation further complicated by the production and O 2 ratherthan other forms of ROS. ROS comprise a set of chemically .

ding H (Winterbourn, 2014) The fluoresceinThe probes,for example dihydrofluorescein diacetate (H

(Gilroy 2 O - 2 diaminobenzidine) arefairly specificfor H 2 O

. (Kristiansen ), a), radical signalling molecule (Fig. At 1). the same timeproblem the of

2 et al.et

metabolism and signallingreliable is measurement high with temporal

the , 2016) - literature refers to the involvement unspecifiedof encoded probes with imp

ism and signalling roles. To do this wefocus specifically as as function and geneexpression. To critically assess the functions ht. All rightsht. All reserved. H 2

DCFDA) etal. . Surprisingly, these warnings arelargely ignored and . Thewidely - H

2 (Winterbourn, 2014) DCFDA) react with a wide range r of , 2009; Šnyrychová - H

and 5 2

DCFDA hasbeen made - 2

based compounds should be usedwith care for O 2

- and superoxidetoxicity (Section III), the - used methods for measuring H (and - VI)and functions its in terms of - 6) chloromethyl 6)

Fig. roved specificity

et al.et and reactive sulfur species

1

illustrates thepathways H of 2 O , 2009; Schmitt 2

butrequire peroxidase (Kristiansen - 2’,7’ 2

O (Section II) 2 adical

measurement tuation is largely a - distinctspecies 2 . -

2 ) hence) et al.et et al.et O - based ROS in 2 2 an FDA), . H , 2014; , 2009). d other d other

(DeLeon 2 it can O 2',7' 2 2 is O

2 -

This article isprotected bycopyrig Acceptedhas beensuccessfully stage inArabidopsis Exposito removing itsability to respond to H requiringuse the aof control such as SypHer, inwhich one of t Rodrigues Exposito HyPer and its variants have been widely fluorescence excitation ratio theof attached YFP, for oxidationH by hydrogen peroxide 2014) versions suchas HyPer thewas first genetically probeencoded with high specificity for H accessibility to substrates andpotential, redox providing specificity some to their oxidation. HyPer Grx1 improved coupling to GSH/GSSG,latest the version of roGFP2 is attached to glutaredoxin producing differentsubcellular compartments glutathioneredox state (GSH)inratiometric a manner and ha usedwidely GFP Articlea high potential to solvesome of the problems associated with small molecule probes. Thefirst Genetically production extraction of tissue samples in plants,which range from 50 in tissue extractsis fraught with technical difficulty, leaving no consensus averageof concentrations (Winterbourn, 2014) widely an alternative visualisation. Luminol, which produceschemiluminescence when oxidised has been electron microscopy probefor H hasprobes been critically evaluated - roGFP2 . HyPer constructedwas incorporating by OxyR into - used to measure theextracellular “oxidativeburst” buthas complex a chemistry - - Rodriguez Rodriguez

etal. - 2 and encoded probes inwhich fluorescent proteins havebeen engineered detectto H O

(Gutscher 2 . Cerium (Ce

, 2017; Mullineaux scavenging. - based sensors (roGFP1 and 2) were modified withcysteine a pair to respond to 2 O -

sensitivetranscription factor, which contains a cysteinepair with high specificity et al. et al.

2 (Exposito . Finally, even the apparently simple task of measuring the H (Voothuluru Sharp, & 2013)

- resulting inadisulfidebond. The thiol targeted to peroxisomes -

3 and3 et al. , 2017) , 2013; Hernánde 3+

does notreveal ) forms) insoluble Ce(IV) perhydroxide which can be visualised by , 2008) HyPerRed - - Rodriguez 5000 nmol g . In somecases HyPer is prone to silencing beyondcotyledon the

et al.et 2

. The environmentof cysteines in

(Schwarzlander O (Šnyrychová ht. All rightsht. All reserved. 2

butmaintaining pH response , 2018) - havebeen developed used invarious systems including plants

et al.et z - - Barrera

1 the cellular and organellespecificities H for

fresh weight , 2013) . (Costa However,it has disadvantage a in being pH sensitive,

but confocal reflectance mi etal. allowingprobe the to beused ratiometrically.

et al. etal.

which could limituse its in plants. However,it et al.et , 2009) , 2015; Exposito , 2008; Bratt circularly permuted (Noctor , 2010) - disulfideinterconversion changes the . Cerium chlorideis a potentiallyuseful ve been ve well validated in plantsin

(Bilan hecysteines has been replaced, 2

O and multiplesubcellular et al.et

2

et al.et (Matlashov

(Belousov

proteins determines their et , 2016) al. - , 2013; Ermakova Rodriguez , 2016) croscopy might provide YFP. OxyR is an .

etal. Moreover,

et al.et

(Costa . 2

O To provide

et al.et 2 , 2006)

, 201 co

2 et al.et ncentration O , 2017; 2 5;

the etal.

and 2 , 2010; O E. coli 2

have , new

This article isprotected bycopyrig AcceptedProchlorococcus natural example of the importanceof defenceagainst H antioxidant systems, particularlywhen pushed to the limit by environmental stresses.A striking removing superoxideand H nM) curve Valishkevych, 2016) occurs at micromolar butnot low millimolar Arabidopsis III. 2017) modification apoplastas the and lumen ER wherethe probelikely is to b current genetically activity theof antioxidant system concentration as observed for A po theso extent to which thesespecies interfere with Articlesystem. HyPer re external H H of not measureabsolute concentrations since the oxidation state theof probe is dependent on the rate Although genetically roGFP2 pH is not sensitive. Other variantsof H roGFP2 with the yeast peroxidasethiol Following fro compartments Hydrogen peroxide 2 tential disadvantage of constitutively expressed probesis that they could disturb H are remarkably similar O . Estimates for resting intracellular H .

2

- production (Gutscher

- peroxiredoxin Thiol peroxidases reactalso with lipid hydroperoxidesand peroxinitrite reduction after a H 2 O growth is inhibited by 1 mM H 2 m HyPer,m new sensors based redoxon relays arebeing designed. A fusion of roGFP2 of

additions can calibrateHyPer

by HyPer(TriPer) is able to operatein the lumen ER of mammalian cells , which

transient expression in et al.et - encoded proteinsunlikely are to work well in more oxidising compartments such versus

and thedata Claeysof - encoded sensors provide specificity and temporal i -

, 2009; Scuffi based probe andsuperoxide toxicity lackscatalase

thecapacity 2 (Seaver Imlay,& O 2 O 2 E. coli 2

is made clear is made byimpaired the function of mutantswith compromised (TPX)

exposure could exposure provideinformation aboutthe capacity of the thi . This problem could beavoided by inducible expression. The

(Ermakova

etal. (Lim Orp1 (roGFP2 - ht. All rightsht. All reserved. peroxidase(KatG). cannot It grow unless naturally 2 and rate O 2

Nicotiana benthamiana

, 2018) etal. 2 sensors not reportedyet inplants are HyPerRed and a 2 O et al.et O

(Huang & Sikes, 2014)

2 2001; Huang, concentrations 2

concentrations in (Claeys , 2014)

et al. of theof systemthiol to reduce the probe. Using

. roGFP2 (2014)also providehint a of this com

- H Orp1)allows H , 2014; Morgan 2

O

et al.et and could causelonger term changes int 2 2

measurement O - Orp1promising is because,unlike HyPer,it 2 BK , 2014)

ecome fully oxidised.

is illustrated by the pico (Nakamura

et al.

E. coli (Exposito

. and observing the kinetics of 2 , 2016) I O n mammals and yeast

etal. 2

- and mammalian cells dependent oxidation of in vivo

et al. nformation H on , 2016) . requirementThe for - Rodriguez , 2003; Semchyshyn &

requires investigation. . (Mul A recent

-

cyanob (Melo ler plexresponse et al.et 2

O - etal. 2 occurring

O 2 toxicity

2 et al. , 2017) acterium

(20 they dothey , 2017) - he 35 ,

ol ol .

This article isprotected bycopyrig as damage,two points are worth bearing in mind. Firstly,proteins contain sufficient methionine (Bechtold the various isoforms are more sensitive to high lightand increased show metabolicdisruption B type isoforms which use thioredoxin glutaredoxinor r as methionine high lightand ambient CO been identified in Arabidopsis catalase( constant (Table 1) and, consistent with reactionThe between methionineand H (Wheeler superoxide SOD mutants Ascorbatesupplementation rescues oxygen sensitivity, lifespan and amino acid auxotrophy of yeast showed that mitochondrial MnSOD is essential for female gametogenesis (Martinal., et 2013). leastat being consistent with FeStargetingsuperoxide. by theof TCA cycleenzymes aconitase and isocitrate dehydrogenase 2011) bleaching, while the cytosolicFSD1 KO had no obvious phenotype is cytosolic/nuclear. Knockouts of (Chu Hekimi,& 2009) oxidativestress and sometimes have decreased lifespan apoplast CuZnor and yeast SOD mutants susceptible to and H 2003; Wilkins (Section term toxicity H 2 Accepted Article O 2

et al.et is removed by “helper” bacteria “oxidative stress”. . Mitochondrial MnSOD 2 O in plantshave not been extensively studied and theireffectshidden are withinblanket the 2 and arepresent in cytosol, chloroplast, mitochondria, peroxisomes VI

(Kim

toxicity

et al. et al. , 2005) ) is induced) and has physiological significancein pollen . Arabidopsis contains least at type5 A peptide methioninesulfoxide reductases and 9 dismutation to H

(Zyracka et al. et al. demetallation , 2015) , 2009; Laugier . Arabidopsis . Of the threeFeSODs inArabidopsis, two are chloroplastic (FSD2 and 3) whileFSD1 in plants. , 2011) , 2008)

buffersthem againstthe more severesymptoms of SOD deficiency. et al.et

(Imlay,2013) ( Fig. . 2 . SOD mutants from yeast,flies and mice are usually more sensitive to

I P (J , 2005) t is nott known if thereare specifically

2 roteins c acques 1).

by both superoxideand H O lacking Cu/ZnSOD activity grow

antisense lines et al.et 2

In somecases programmed cell death or autophagy of

(Table 1).is possible It that high ascorbate concentration

thetwo chloroplast isoforms causeslight sensitivity and severe

presumably becauseof appreciable its rate constant for , 2013)

et al.

ontaining FeS clusters and mononuclear iron centres are ht. All rightsht. All reserved. (Table 1). SODs area diverse setof enzymes containing Fe, Mn (Morris

this, cat2 2 O , 2015) . While methioninesulfoxide production generally is seen 2 , forming methioninesulfoxide, hasa relatively largerate ~ ) mutants that accumulateexcess H

havesomewhat impaired growth andinhibition show 400 proteins containing methionine sulfoxide have etal. . Methioninesulfoxide reductase , 2011) 2 O although 2 .

eductant leading amino acid to auxotrophy in The characterisationThe of knockout mut Specific t s

normally under laboratory conditions - - sensitive targets for superoxide notin stigma incompatibility (Morgan (Myouga argets of superoxideand H (Laugier C. elegans

et al.et etal. (Pilon

etal. 2 , 2008) O , 2008; Zhang

, 2013) regenerates et al.et 2

(Van Raamsdonk when exposed to , 2011) organelles , theformer . Mutants in (Dat

in

plants

et al.et

and 2 etal. E. coli O ants 2

, ,

This article isprotected bycopyrig covered in the following sections dependent protein must provide light/dark or circadian cues. signalling peroxisomal acyl enzymescould also generate Arabidopsis and Drosophila dependent manner. ROS (H carefully controlled. Flavin containing proteins arepotentially able to reduce oxygen inblue a light dihydrofluorescein dyes oxidisesthem, so investigations involving lightand ROS production mustbe potential concern in microscopy when R laboratory Consequently, nanomolar to low micromolar concentrations arefound inthe environment and H IV. reactive electrophile species (RES) evidenced by mutagenesis in Hydroxyl radicals initiate lipid peroxidation and cause protein carbonylation and DNA damageas generated by release of Fe reaction or Haber except inthiol peroxidases (Winterbourn, 2015) Superoxide physiological significance of methi the possibility of effects on susceptible methionine residuesnear phosphorylation in sites human the proteomegiving rise to oxidation nearbyof methionineresidues and therean is over system residuesfor them toused be catalytically 2 O

Accepted Article Productionofhydrogen 2

forms spontaneouslyforms from the interaction between water, organic matter and light. (Levine

(Bodvard

(Li (Li Imlay,& 2018) can react with

et al.et - CoA oxidaseis impaired in light - Weissreaction (

et al.et , 1996)

(Table 1) , 2017)

cysteinethiols to produce reactiveand undesirablethiyl radicals 3+ . . Secondly, serineand th

2 metabolic activity signallingor H (Consentino

O . Photochemical reactions producing superoxide and H from proteins followed byreduction its with superoxide or ascorbate. 2 E. coli O

2

O peroxide: enzymes peroxide: subcellularand locations but th ) production) from cryptoch 2 . Since yeas 2 . -

can give risecan give to thehighly reactive hydroxyl radical inFenton the and then and summarized in onine oxidation remainsestablished. to be Fig. are

SOD mutants eir significance ht. All rightsht. All reserved.

1). 1). formerThe reaction requires free Cu signalling molecules

O et al.et via S probesare being used. Illuminating the H t lackst conventional photoreceptors, flavinanother 2

methioninesulfoxide reductase O , 2015; 2

in the lightand, it shownwas thata - induced H (Imlay, 2008) reoninephosphorylation is influenced by in vivo Arthaut Fig.

2 rome,a blue lightphotoreceptor, . (Veredas

is unknown. (Farmer & Mueller, 2013) 2

O

-

et al.et

T representation of oxidation 2 . Lipid peroxidationa results range of

he routes production and downstream , 2017)

etal.

H , 2017) of H of 2 .

O Other flavin 2

is poorly reactive, 2 as an H O +

2

or Fe .

production However, the 2

O yeast mutant in 2 . 2+

O 2 -

. Fe are also aare also 2 containing

removing 2+

occurs inoccurs could be are - This article isprotected bycopyrig Accepted Article 1. 2.

production activates NADPH transport (CET)has a simila instead of H al. photoreduction hasbeen identified in cyanobacteria, green algae and bryophytes oxygen to water production. photoreduction havebeen proposed which could actas “valves” to decrease H involvespecific proteins, this may repay consideration. Alternativeroutes of oxygen peroxidases( located superoxidedismutase reaction inhibitor DCMU suggesting isthat it formed downstream of PSII, mostlikely in the Mehler that most theof H (Mubarakshina Borisova has beendocumented from proportion electronsof reducing oxygen to form superoxideat PSI (Mehler reaction) vary photosystems chloroplaststhere are multiple potential sites superoxideof production conditions provide opportunitiesfor H production Chloroplasts and mitochondria source of NO of oilseeds ing forlikely photorespiration purinecatabolism, and synthesis someof hor photorespiration (glycolate oxidase), fatty acid oxidation (acyl site duringdepending catalysis redox on potential and degree solventof exposure of the active dehydrogenases vary considerablyin therelative amounts superoxideof reaction”“side specialised for compartmenting oxidase enzymes which produce superoxideand H Peroxisomes and glyoxysomes , 2017; Shimakawa

(Messner Imlay,& 2002) 1 - 5%

(Exposito (Mullineaux

of largeof electrochemical gradients across energytransducing membranes. These 2 P O . S

lastid terminal as well ection 2 1 and 2 (PSI and and PSII) the lyoxysomes,specialised a type peroxisomeof

. FDPs . FDPs are lacking inangiosperms whereit is suggested that cyclic electron (del Rio & Lopez but more recently a - 2 Rodriguez O 2 , VI

et al. providingpossibility the peroxinitriteof formation. productionblocked is byphotosynthetic the electron transport

in situ ). et al.

et al. Al

(Queval , 2017) thoughis it tacitly assumedthe that Mehler reaction doesnot r protectivefunction

- , 2018) oxidase(PTOX) accepts electrons from plastoquinol and reduces . In plants, superoxide/H

, inisolated chloroplasts and thylakoid membranes dependent CET et al.et ht. All rightsht. All reserved. , 2012) assistconversion to H are organelles - are sites of intenseelectron transportactivity coupled with Huertas, 2016) . , 2017)

FDPs take electrons from PSI and reduce oxygen to water et al.et

Oxygen photoreduction . role Recently, the useof stroma 2 O , 2007) 2 .

for generation Stromal electron transport chain

(Strand flavodiiron proteins (FDPs)in oxygen mones. Largefluxes of H boundeda single by membraneand

. Flavin and

(Chaux

and thylakoid membrane(stromal side)

fatty acidutilisation during germination 2

etal. O

2

via O - 2 containing oxidases and

2 et al.et followed by reduction to water by

forming oxidases are involved in superoxide dismutation , 2015) . produ , 2017) Peroxisomesappear be to a - CoA oxidase), polyamineand . - M targeted HyPer hasshown cing . Relevantto this, H itochondria generate (ETC) 2 O

superoxideand such as 2

and H

are particularly . Estimates theof 2 2 O O

. In 2 2

(Chaux

2 produced O 2

as a 2

H O

et 2 2 O

- 2

This article isprotected bycopyrig Accepted Article 3.

have beenhave extensively reviewed and DAMPs). Molecular mechanisms activating NOX hormones (ABA, ethylene) and pathogen and damage associated mol production inapoplast the is induceda by plethora of stimuli suchextracellular as ATP, activation has been demonstrated 2014) the PM or ER example salt stress,superoxide/H regulatory proteins sensor kinases. mediated H membranepermeable, the proposed signalling roles for NOXs either require aquaporin and corroborativeevidence are needed. Given that superoxideboth is short specific not to NOX NOX functions but many studies have usedtheinhibitor diphenyleneiodonium (DPI) which is just not about be superoxide the extracellular space will depolarise the membrane, dismutation could increase apoplastic pH, activity perhaps using germin reactionfavoured is by low apoplastic pH butthere is also evidencefor apoplasticSOD Su 3). electrons to cytochromeslocated inchannel a formedthe by transmembranedomains ( andtermini. C The C superoxide inthe plasma membrane enzymes which use electrons from cytosolicNADPH to reduce oxygen to mammalian enzyme inthe neut (NOX). NOXsPlant apoplast and the complexityillustrated is in Plasma membrane and apopla Riemer complexesI, II and II superoxide and H peroxideproduction is followedits by rapid dismutation H to . N The

etal. 2 O , 2015; Huang, S - terminus ofhas NOXCa (Leshem 2

transport to the cytosol interactionor its of products wi Localisation inlipidcould rafts facilitatetheir interaction with potential

2 apoplast. Models predictsix membranespanning domains with cytosolicN O are

asis it a general (Hao 2 -

and flavin containing terminus hasbinding for sites NADPH and FAD. Reduced FADtransfers throughelectron the transport chain particularlythrough

et al.et named respiratory burst oxidasehomologues (RBOH) after the

et al. , 2

- (Segal, 2016) ht. All rightsht. All reserved. et al.et like proteins. The proton consumptionsuperoxid by 006) , 2014; Nagano st. st. rophil microbial defencesystem

(Qi 2 There are numerous routesto H , 2016) O

in vivo and RBOHDis internalised into PM vesicles

etal. 2 flavoprotein

2+ production occurs in cytoplasmic vesicles - binding and handmotifs EF Ca , 2017)

. (Potocky

. Mutants beenhave dehydrogenases and the RBOH

Fig.

et al.

3. Aprominent3. sourceNADPH is oxidase

and involvereceptor inhibitor

, 2016) et al. via

so thatso

its regulatory N , 2012) - mediated transport of electron to

. Undersome conditions, for (Riganti

(Schwarzlander NADPH oxidase . NOX important

(Segal, 2016) 2 et al. 2 O O - 2 2 - ecular patterns (PAMPS dependent ROS

. Thisproton 2+ likekinases (RLKs), production inthe th extr , 2004) - - dep terminal domain

for understanding

et al. - endent lived and poorly . NOXs are

acellular function might

, cautionso (Hao respiratory derived from , 2009; e - requiring

etal. - Fig. ,

This article isprotected bycopyrig Accepted peroxidase with the suppression of H causingpH a increasealso elicit “ROS” production elicitor/PAMP responses. In potato, comparison of various PAMPs and DAMPs shows that only those described by Bolwell growth (Daudi suggestsrole a for peroxidasesin thegeneration H of favouredhigh by pH and requiresreductant a Daudi radicals depending on the chemical environment ( (Section contains numerous typeIII peroxidaseisoenzymes with functions in cross NOX hasreceived high profileattention butthere are other sources apoplasticof H Article

et al.et

et al.

(Sundaravelpandian influences on developmental defects as well as pathogen sensitivity Antisensesuppression of thetomato RBOH family produced plants with multiple surprising not that NOX mutants are relatively signalling events for which seminal work theon role of NOXinroothair growth in polargrowth is conserved across brown seaweeds, fungi and mammals but,following the involved in stomatal function and pathogen responses responses and systemic signalling (Foreman RBOHC and RBOHH/J function inpolar growth rootof hairs and pollen tubesrespectively extent in Table protein kinases (e.g. BIK1) and GTPases small (RAC/ROP). phosphatidic acid,

VII - ). However peroxidases are repo , 2012; Kimura derived H , 2012)

they arespecialised specificfor functions ina widerange processes.of For example, 2 .

(Rentel (Rentel etal.

, stomatal defences Arabidopsis hasisoforms 10 NOX with distinctexpression patterns and some to ’s group 2 root O , 2 2003; Boisson

production for “ROS” production NOX is required seem still obscure. Cell wallremodelling ( + et al.et

- et al.et calcium influxactivating calcium developmentstill are coming to light ATPase

et al.et

is favoured by high pH consistent with thepH increasesreported durin , 2004) , 2014) , 2013; Mangano

activity ht. All rightsht. All reserved.

are candidates. Consistent with these mult . H The -

(Khokon Dernier

(Miller REF), rted to variously 2

which hasnot been identified. The ofuse mutants O

etal.

2 could etal.

generating reaction is notfully understood butis etal. Fig.

(Moroz et al. , 2013; Kaya, H. , 2010; Arnaud 2

O contribute to 3) , 2009) susceptible to environmental changes 2 , 2017)

(Chen & Schopfer, 1999; Kawano, 2003; or otherROSor duringimmune the response ? et al.et -

dependent protein kinases(CPKs),

(F generatesuperoxide, H . RBOHD andalso Fare variously

(Sagi oreman . (Kadota , 2017)

The H The (Orman

Examples and referencesare given

etal.

the high pH to favour etal. et al. 2 . Isit feasibleNOX that

O

et al. etal. - 2 Ligeza , 2004)

, 2014) , 2017) production reaction linking cell wall polymers , 2003) , 2015)

et al.et , while more , RBOHD in wound ,

andhair root iple functions,is it

2 . The role NOXof the S O 2 , ection

O 2 2016) . 2

biochemical

The cell The wall and hydroxyl type III . VII

. , along ) or

g This article isprotected bycopyrig which are secret andinsects microbes. production by nectaries and trichomes consequencesfor growth, lignification, pathogen defenceand signalling peroxidase, CuAO,PAO, oxidised ascorbate) and removal (peroxidase) is emerging along with thereforeinfluence H Cell wall ascorbate oxidase maintains ascorbate ina relatively oxidised state,and its activity could unidentified oxidation productof ascorbate also inhibits peroxidase activity wi ascorbate(dehydroascorbate and 2,3 ascorbateof degradation incell the wall butis it also potentially relevantthat oxidation products of oxala and CO Someplants, for example cereals, contain apoplastic oxalate oxidase(germin) which produces H products formed by amine oxidases havenot been considered. tubes H reactivespecies Mutants or over 2016) apoplasticalso (PAO1). They havewide substrate specificity for polyamines Arabidopsis) are largely apoplastic, while PAOs (5 genesin Arabidopsis)are largelyperoxisomal but flavin (FAD) A number of other oxidaseslocated are in theapoplast including copper amine oxidases(CuAO), 2 O Acceptedth non Article 2 4. - te oxidase activity dependent stomatal

. Products amineof and

(Wu 2 producethe disulfide form a of 2 This process therefore generates H PDI, which in turn transfersdisulphide the bond to target proteins induceto correct folding. produces (ERO) anendo involveH bonds. The two means of oxidative cross linking which facilitates the protein folding processes that depend the on formation disulfideof Endoplasmic reticulum (Le (Le Deunff - enzymaticH

et al.et - dependent polyamineoxidases (PAO)and

, 2010) - and use of mutants and polyaminefeeding suggests that they contribute to ABA and ed into the nectar anda nectary by NOX expression of various apoplasticamine oxidases confirm anincrease decreaseor in 2 O

etal. 2

(Bulleid, 2012) 2

2 Nectar O O . Thepote

(Membré 2 2 , 2004)

production. Overa production closure

H polyamine 2 . Arabidopsis hasafamily germinof . TheisER an oxidising compartment O - ntial signalling roles theof reactivealdehydes and theirfurther disulfideby reducing oxygen H to

2

et al.et

(An (~30 . Infirst, the a FAD

(Kärkönen - ht. All rightsht. All reserved.

diketogulonate) candegraded be under apoplastic conditions et al.et , 2000) (Peiffer µ

- oxidation are M) M) Cys peroxiredoxin or the sulfenic acid form of a glutathione 2 , 2008; Gémes ll, a complex pictureof H O is formed 2

. In contrast, thesecond mechanism uses H b

et al.et ut which may haveSOD activity. Oxalatea product is

et al.et , 2009) , 2017) - via oxalate oxidase. CuAOs (~ genes10 in H co 2 via

O (Bezzi ntaining endoplasmicreticulum oxidase

glucose oxidase and a germin et al.et 2

protein disulfide isomerases (PDIs) both a . may contribute to defence against nd analdehydeor amino aldehyde. Very interestingly, a currently

, 2016)

et al.et 2 - O likeproteins, which do nothave 2 , 2010; Harper 2 for glutathioneand thiol groups O . Oxidised ERO then oxidises

and H 2

production (NOX, (Fig

(Tavladoraki (Kärkönen 2 3 O ) . 2

Extracellular production in pollen

et al.et

etal. -

like protein , 2010) etal. 2 O , 2017) 2 H

to to , 2 O .

2 2 O

2 .

This article isprotected bycopyrig maiz in yeast between AtPIP2;1 is phosphorylatedOST1 by inresponseto ABA inbothrole waterand H induced stomatal closureand the apparentlymutants decreasedhave intracellular suggesting ROS a intracellular H movement inthe allowsmutant increased bacterial growth, presumablyby int H selectivity for H aquaporins usedby water are involved in H evidencefor the aquaporin dependence of an e activates the redox controlled transcription factor NF characterised. A mouseaquaporin 3 mutantimpaired is in NOX2/H al.et (PIPs)and tonoplast(TIPs) andlikely most inthe chloroplast inner envelope channel proteins t of Like water,H V. 2 O

Accepted peroxideHydrogen transport Article 2 e roots,e implying that a possible oxidative modification to aquaporins decreasestheir water

, 2012; Bienert Chaumont,& movement from theapoplast to the cytosol during PAMP

in plantsis required. bond form dehydroascorbate, the oxidised form ascorbate,of in the ER could also facilitate disulfide removal of H the ER membrane in role storageprotein synthesis whichER/chloroplast is local (GPXL) extensive formation disulphideof links the EROpathway indeveloping soybean seedlings wherestorage protein synthesis involves an ER While the Arabid peroxidase( (Bienert maize plasmamaize membraneaquaporins inH 2 - O 2 localised peroxiredoxin (Aller and Meyer, 2013). O pathway 2 2

O

2 is relatively poor atpermeating membranesand its transportis facilitated by et al.et

signalling 2 ation. Further investigation of the oxidative processes involved in protein folding

or or may beimpermeable to H G he aquaporin type. Plant aquaporinspresent are theon plasma membrane 2 O P , 2014) X 2

) which) then oxidise In plantsPDI. is it not known ifboth pathways operate. 2 in plants produced by the ERO system. Finally, investigated,but not the presence of opsis genomeopsis contain O

(Attacha 2

(Tian transport . High H

e is supported by theobservation that rice mutantsin OsGPX 2014) t al.

et al.et ised, has noticeablydecreased grain filling, consistentwith a 2 O ht. All rightsht. All reserved.

(Grondin , 2016) 2

. Their presence otheron membranes is not well

concentration (~30 mM)decreases waterpermeability of , 2017) (Matsusaki 2 O . 2 At

s transportbut some forms may havegreater

(Matsusaki ntireH . GPX etal.

2 2 ERO2 and 13 PDIproteins, p O ip2;1 2 2

O (Almasalmeh et al. , 2015; Rodr L - 2  s

2 permeability was demonstrated by expression

O B

mutants aremutants impaired in ABA or peroxiredoxins could be involved in (Grondin 2 (Hara , 2016)

signalling system. Most likely the same

et al.et

- - However,there is strong evidencefor triggered immunity. Decreased H Chikuma , 2016) . Arabidopsis GPX

igues

etal. et al.et 2 O 2 -

, 2015) , 2014) etal. . The possibility of a GPX mediated signalling which

et al.et

, 2017) there isthere no evidence for (Mubarakshina Borisova . . AtPIP1;4 facilitates , 2015) Thedifferences erfering with L . Int 3 is 3 attached to - , providing

and PAMP erestingly, - L 5, - like - 2 O 2

This article isprotected bycopyrig Acceptedtranslational modification has beenreported. Thereare numerous reports increasedof r increase inresponseto stressand insome cases control theirof enzyme activity by post H to likelymost restricted to peroxisomes. Ina nutshell, knockout mutants are generally moresensitive peroxidaseshave numerous isoforms and arefound inall subcellular compartmentswhile CATis theof peroxidases havebeen extensively reviewed are also GPX thioredoxin as reductant peroxidasesinclude peroxiredoxins plantscan develop very high ascorbateconcentrations inphotosynthetic tissues. thiolThe 2015) photosynthetic organisms but,along with ascorbate, are absent from cyanobacteria and ascorbateperoxidase (APX) and typeIII peroxidases. APXs arestrongly restricted to peroxihaem Most organisms contain multiple enzymes to remove H VI. Articleconf (Hara areAP3 physically associated which would facilitate movement H of 2016) andER cytosol is likelymost facilitated by aquaporins in mammalian cells investigated in this regard, little is known theirof role in other membranes. H aquaporins could influence lightsignalling. While the plasma membrane aquaporinsbeen have Rodriguez al.et acetazolamide, photosyntheticelectron transport permeability aquaporinsof very is dynamicand could influenceH AtPIP2;1 beto internalised in endosomes permeability Control of hydrogen peroxideconcentration:and how where? L 2 i rmation inplantsand will , 2012) O s -

. Compared to animals, whereascorbate is not considered as a major player in H Chikuma buthas notbeen investigated inplants. Furthermore,in mammals NOX2 and 2 also

and stres candidates for H

et al. react with . Since dasesand thiol

(Ye (Ye Steudle,& 2006)

et al.et , 2017) a membrane sesare that expected to increaseH chloroplast , 2015) o , it rganic hydroperoxidesand

2

(Iqbal O is possible that expression or gating of specific chloroplastenvelope 2 . -

based - sensing (Section The functionThe aquaporinsof in impermeable reagent thatblocks aquaporins - sourced H

require et al.et . Interestingly,lower a concentration H of - peroxidases. Inplants,the haem peroxidasesare catalase (CAT) sourced H Prx , 2006; Navrot ht. All rightsht. All reserved.

the careful use of mutants and inhibitors

and glutathioneperoxidase 2

O (Wudick 2

influences nuclear H

2 VIII O 2

). The subcellular locations, properties and functions from isolated chloroplastsblocked is by

phospho etal.

et al. (Dietz, 2016; Maruta 2 O 2 2

, 2015) load. Transcripts some,of but not all, O , 2006; Attacha 2

H with twodistinct reaction mechanisms: lipid hydroperoxides. peroxidases Thiol 2 O

. Itappears that distribution and 2

transport 2 2 O O - 2 like 2 2

O and gene expression signalling.exit The of 2

into into the cytosol for signalling (GPX etal.

etal.

(Appenzeller needs furt

(Mubarakshina Borisova 2 O L , 2017) 2 ) enzyme 2 , 2016) O

(0.5mM) causes . 2

transpor

the aquaporin . her (Wheeler . Besides H

APX and thiol 2 - s which O Herzog - esistanceto 2

t betweent removal, (Exposito

et al.et et al.et use 2 O 2

,

- , ,

This article isprotected bycopyrig Accepted Article 2016) stress resultas a of over 1. .

evidenceso far, i peroxisomesproducing are photorespiratory H catalase inperoxisomes plantsfloating H on evidencethat peroxisomesa are sinkfor H antisense or co peroxisomes was not determined. Contrary to peroxisomesacting a as so by DAB staining inintactleaves. However,this evidenceis weakbecause its sourcefrom al. supported by physical association between catalase and glycolate oxidasein rice resultssuggest that close enzyme association allows metabolitechannelling andalso is physical association spinachof peroxisomal leaf enzymes dueto closeinteraction of enzymes. Insupport thisof hypothesis (Heupel surprisingly (Mueller, 2000) peroxisomes actively oxidising acids fatty release H from peroxisomes 2016) they could also function as H assumption that peroxisomesevolved to removeor contain H peroxiredoxin in photorespiratory H peroxisomal APX3 mutant shows no obvious phenotypelowat lightintensity at which Addit Arabi the ultimate reductant). Peroxisomal catalase mutants been have extensively studied in removed without perturbingcellular the redoxstate (i.e. GSH and NADPH are not needed as affinity for H 1997) peroxisomes, to the extentit that is often associated Peroxisomes and glyoxysomes. ,

2016) dopsis and tobacco andits show key rolein H ionally to catalase, . Kinetic modelling of H .This high concentrationperhaps is required becausecatalase does not havea high

et al. . Salicylic aciddisruptsthis association and causesa small increase inH it appears to berelatively impermeablebased on catalaselatency assays 2 O , 1991) 2 - . . However, catalase is “ideal” inthe sensethat a largeflux of H suppression of - T t will beimportant to determineif peroxisomes are always net sinksor if plant expressing peroxidases, of particularlyAPX heperoxisomal membrane

(Poole, 1975) 2 2 O O . Therefore, retention inperoxisome the would be aided by channelling 2 2

peroxisomes

production wouldlow be solution depleted it fasterthan could APX 2 2 ht. All rightsht. All reserved. O is O act as aact sinkfor extra CAT1 2 2 also associated peroxisomes. with In Arabidopsis, a

Catalase sources, particularly sources, f and, inbroad supportof thisprediction, isolatedliver rat production predicts that5% of H (Corpas , the major catalaseisoform in tobacco, provided

is present in 2 O

etal. 2 is

(Willekens

2 has O

(Narendra , 2017) 2 . 2

2 Given the poreslarge enough to allow O - O peroxisomal H

2 with crystalline structures 2

or signallingor very high concentration in

removal albeitat very lowconcentr CAT1 CAT1

requires corroboration.

et al.et (Heupel Heldt,& 1

et al.et

(Dietz, 2016; Maruta al.,et deficient mutants. Therefore contradictory natureof the 2 , 1997) O

(Queval 2 , 2006) , 2

thereis evidencefor

O it hasbeensuggested that (d 2 O 2

el Rio & Lopez produced would leak 2 . Leaf discs o

even when the

. etal. The single report of urce of H 994) , 2007) 2 O

(Kleff H 2

. These 2 O (Zhang Despitethe 2 ation

f wild is O 2 2 - O

. Huertas, detected 2

2

loss butloss , etal. -

type et , This article isprotected bycopyrig Accepted Article 2.

P stroma (sAPX) and attached to the thylakoid membrane(tAPX) photosynt ascorbate) and peroxidasesthiol which together removeH Chloroplasts. Kneeshaw which could resultin controlled H that catalaseactivity can bemodulated a by number interactionsof and modifications, had somewhathigher H butno dependent protein kinase CPK8 dependent manner interact with LSD1,zinc a fingerprotein which is involved in cell death inpotentially a SA al.et seems thatphysiological concentrations SA wouldof betoo lowfor directinhibition acid suggesting the possibility thatH are degraded severely high H Arabidopsis CAT2 and maintains catalaseactivity leaves absorption. Itis continuouslydegraded and synthesised inalight metabolitesneeds to be addressed. Catalaseis sensitive photoinactivationto chloroplasts the peroxisomal membranebegated? A subset of peroxisomesare also attached to peroxisomal responsesincrease the H perhapsso proliferation is necessary butnot s promoting peroxisome proliferation does notincrease salt tolerance al.et mobility under ox peroxisomeactivity that will impinge thisquestionon are proliferation and increased peroxisome they can alsosources. be Interestinglystrong evidence a for specific signalling rolefor rx , GPX , 1995) , 2016)

t int the peroxisomes (Engel L 1 and1 7 are prominent thiol peroxidases inArabidopsis heticelectron transport et al. - . Sa

but indirect interaction may occur sourced H (Gao

et al.et by autophagy The key componentsare APX (andhigh a concentration of its substrate 2 ltstress peroxisomecauses proliferation, butoverexpression of PEX11 , 2017) O

idative stresses and formation peroxuleof extensions 2 et al.et

, 2006) production, for examplein

(Li

2 . etal. , 2016) O

2 O 2

andcytosolic a chaperone protein (NCA1) which interacts with 2 is demonstrated in y

as determined by BiFC assay leveldetermined as by DAB andprobes. DCF Itis therefore , 2015) (Shibata ht. All rightsht. All reserved.

andpotential the for channelled movement H of , although 2 O via . CAT3phosphorylated is and activated by the calcium 2

2

etal. O releasefrom peroxisomes

2 FDX O 2

2 will increaseduring responses. defence However, it

their source sinkor and can channels for H , 2013) both proteins as theultimate reductant. APXhas isoforms inthe ufficientfor salt tolerance. Do these cat2 east (Yuan

. Catalaseand APXare inhibited salicylic by (Li ,

(Bodvard

peroxisomesbecome aggregated and et al.

etal.

interact (Zou , 2015) , 2017) 2 O

2 et al.et et al.

using NADPH

(Maruta

(Costa . Underconditions of

in the nucleus and cyto (Dietz, 2016; Attacha - . Arabidopsis CAT1, and2 3 dependent m , 2017) , 2015)

(Mitsuya

etal.

(Rodríguez et al. . Other features of . A , 2010; and cpk8 , 2016)

via

et al. 2 annerin O bluelight

2 mutant mutant

- and other Serrano , 2010)

. 2 2 (Ruffer O

et al.et - 2 likely Cys

sol in - - ,

,

This article isprotected bycopyrig Accepted Article 4. 3.

could comprisean H inoccurs vacuolesdoes as a largeproportion theof type III peroxidaseactivity. Vacuoles transporters),inorganic ionswell as as sugars, amino acids and organic acids. Ascorbate around 90% of the cell volume and accumulates secondarycompounds ( Vacuoles asahydrogen peroxide sink. Morgan increasedhave superoxide/H proteins (UCPs) which allowdissipation ofproton the gradient. Mutantsin these processes water (analogous to chloroplast PTOX and flavodiiron reactions features: the alternative oxidase(AOX) which diverts electrons to oxygen and H equivalents producedchloroplasts. by To accommodate these fluxesand preventsuperoxide glycine metabolism as one theof sites photorespirationof (Jiménez glutathioneperoxidase and APXpresent are along with ascorbateand GSH in the matrix Huang, S signallingcase (in the thiolof peroxidases) havebeen well Mitochondria. singletof oxygen. presumably beneficial inremoving the potential for damaged chloroplasts to act as sources mutant can result inautophagic destruction (chlorophagy) with peroxisomes, severe oxidation chloroplastsof in high light,UVB (Kitajima P element through PTMs and geneexpression system. Involvement theof peroxidases thiol also allowsa potential signalling/chaperone synergistically sensitivemore chloroplas sensitivity to photo 2017) rx

by over . APXand ascorbate deficient ( 2 O

2 et al.et

et al.et et al.et etal. production by over ts ists sensitive to photo - oxidation and sAPXbyof H , 2008) , 2016) , 1997) , 2010)

The enzymes re

- oxidativestress buta double mutant of the two 2 . 2

O

. , could allow transient H and onlysome key p

Plantmitochondria areintimately involved in photosynthesis,both in 2

scavenging uptake with facilitated by tonoplast a - 2 ht. All rightsht. All reserved. reduction of the electron transport chain thereare twokey (Awad O moving H 2

- and compromised photos oxidative stress and a triple mutant with tAPXis

etal. vtc 2

O ) mutants inArabidopsis havesomewhat increased In fully expanded cells, the vacuole comprises 2 O 2 , 2015) , whichpotentiated is byspecific a amino acidloop oints areoints summarised here. Peroxiredoxins, 2

in mitochondria and their relationship with (Dietz, 2016) 2 O 2 . This providesa

accumulation allowinga it

. Itis possible that inactivation of -

ynthesis reviewed and in oxidising red (Izumi , Section

multi et al.et

(Sweetlove

- (Riemer radiation and inatAPX - Cys Cys - , 2017) layered IV via

quaporins. A with production of P ) )

rx ct asct a signal. As ABC and uncoupling

et al.et

proteins in and is ucing

etal. H

2 O , 2015; 2

, 2006; removal removal

This article isprotected bycopyrig possibleit is thatscaffolding enzymes of producing and consuming Acceptedare endodermal proteins which provideplatform a for endodermal cell wall modifications. Therefore al.et endodermis lignif apoplastic oxidasesand oxidation. Effects ligninon in mutants could derivefrom either activity. The other that the same(or different) isoenzymes peroxidasecan generate contribute peroxidase.for The source of scavenger impairedhave III type peroxidases formation potentially involves O then reactwith each other produceto polymeris pathogens. Lignification involves their most obvious function inmodifying the cell wall during development in responseor to Some theseof generate ROS (Section extensin and arabinogalactan proteins, contain hydroxyproline residues cell wall or vacuole ArticleRemarkably,Arabidopsis the genome encodes ~65 expressed typeIII hemeperoxidases, targeted to VII. Metabolic hydrogenfunctions peroxide of , 2013) to beto investigated in thiscontext. of lackingmutants vacuole localised peroxidase or with phenolic altered composition need could acta as light this proposal, peroxidaseactivity roseus Shamir, 2013) transported to the cytosol for reduction in exchange for radicalreduced is ascorbate by producing dehydroascorbate (DHA) which could be phenolicsubstrate is oxidisedH by

potassium iodide via . Critically, this process involvesCASP1 which isneeded for localisation of (Sultana

superoxide stem lignification identified all the components this of system ies

(Valério (Marjamaa

using peroxidase(

et al.et . H

2 A detail ascorbate could also beinvolved (Section O H - 2 derived 2 , 2015; Tattini

buffer,extent the of their capacity far so lacks evidence and investigation O

et al.et in spruce cell cultures 2 H

underappropriate

2 ed study of peroxidase and phenolicsubstrates in etal. O 2 (Shigeto , 2004) - oxidation 2 dependent laccases (copper oxidaseenzymes) or

H for for xylem lignificationnot is established. NOX activity could 2 , 2009; Berthet O ht. All rightsht. All reserved. IV 2 PRX

butinvolvement of specificisoforms is not established. Since ) but) they also oxidise a . They are generally N could provide

et al.et et al.et and phenolic 2 64)and NOX (RBOHF)as the

O of of monolignols in the cell wall to form radicals which 2

, 2015) using type III peroxidase.resulting The phenoxyl , 2015) ed lignin. The mechanism of monolignol radical conditions (Section

(Laitinen

et al. . .Lignification inhibited is the by

H While itan is attractiveidea that vacuoles substrate 2 O , 2011) 2

(Ferreres as well as as well catalysing monolignol et al.et -

glycosylated and, like cell wall

widerange sub of . s ascorbate (Fig , 2017) PRX

increase IV

H ). As well as thexylem, the

2 2, 2, IV et al.et O

) it) is tempting to speculate 2 PRX superoxide

(Nguyen

occurs inoccurs other cell types indica , 2011)

during 25 and ting animportant role 2 ) -

. Consistent with

Kim Catharanthus

strates and have drought H (Zipor & Oren / PRX H 2 H O 2 2

PRX O et al.et O 2 H 71 - 2 pro 2 2 -

O dependent source 64. CASPs mutants mutants

2 and , 2016) ducing

high - (Lee .

This article isprotected bycopyrig Accepted ArticleVIII. polysaccharidescission leading cell to wall loosening circumstances, apoplastichydroxyl radicals could take part (Price pathogen responses. Oxidative cross protein which formscross a to the characteristicpat pectins associated with polymerising lignin and possiblywith lignin the itself and this may contribute and response 1. Hydrogen peroxideHydrogen signalling

et al. transmembraneprotein located inthesec signalling, causing oxidation and inactivation (GPX3 system inplants limited evidencefor a complete it hasbeen suggested that these could actas H 2014) disulfideYap1 entersnucleus the whereit actsa as transcription factor prot cysteineforming sulfenic a acid. Thisreacts with its target protein Yap1, forming inter cascade in which a peroxidasethiol (Orp1 activetranscription f react with H peroxidases which contain data. In bacteria, fungi and mammals the em s pathogen responses are well signalling inguard root cells, hair and pollen tube established that production slowsdown. These features makea useful it signalling molecule and itis well (Marinho accumulate Intracellular signalling peculation , 2003) ein disulfide bonds which thenresolve to produce Yap1 with anintra s suchas defence . Plantshave a wide range of L 3) which interacts with ABI2,type a protein2C phosphatase

et al.et . While

on howon transiently 2 O 2 , 2014)

tern cross of (

H (Mullineaux Fig. H 2 O 2 - O H

linked networkwith itself and pectins during wall development and 2 actor, thisso proteinboth is sensor and transducer. Yeast usesa 4)

2 2 . However,it will influencesgene expression across allgroups of organisms. - O . Being moderately long . . In spruce, the cationic peroxidasebinds to negatively charged dependent cross linking restrain will cell expansion, undersome and even form gradients a on cellular scale givenlocalised a source 2 E. coli

sensing and signalling operate low low - -

- linking et al.et linking ht. All rightsht. All reserved. studied proceeesinvolving H

OxyRdirectly is oxidisedH by pKa thiol peroxidase , 2018) thiol peroxidasethiol cysteinethiols

(Laitinen via

be

isodityrosineuses extensin . Apotential example is glutathioneperoxidase )

re scavenged an by the

actsas the sensor andinitially is oxidised on one tory system

erging paradigm for H and enhanced growth (Miao et al.et - 2 lived lived O - based sensing and signal transduction 2 growth, programmed death cell and

in a suitable chemical environment , 2017) sensors. Howeversensors.

in directed reactions et al. s in vivo

insubcellular most compartments and s

(Attacha , 2006)

in plants farexceeds theavailable . Extensina is structural wall 2

O (half 2 2 O

in ways. various However, 2 tioxidantsystem

. GPX anddisulfide the forman is - life ms H to s)

et al.et - 2

(Richards specificperoxidases

O involved in ABA , at thispointis there L 2 3 is 3 most likely a

sensing involvesthiol , 2017)

(Boronat

particularlyin - protein disulfide.

et al.et

so its function 2 O

when its

ABA 2 et al.et

can , 2015) - , to

- like .

This article isprotected bycopyrig tethered to membranes and cytoskeleton show that H locations, including membraneanchored Isoforms of plantGPX (facilitating oxidation theof target), and the subcellular location H of thiol H For These modifications interactwith H otherwiserecycle oxidised CysteinesCRKs. are that H coupled to activation of cytosolickinases. (Idänheimo achievedcysteine by could be caused byprotein a unfolding responseto excessiveH al. (HSFs) canalso be redoxactive and have a wide range targetof genes Heat shockproteins (HSPs) are amongst thoseinduced H by chloroplast in plantsbuta number candidatesof are proposed. Rap2.4ais involved in light 2015) phosphorylation, cysteine ooxidation and, morespeculatively, methionine H known toinvolved be in H kinasehas its activity activatedH by is OXI1 a kinasethat influences roothair growth a 2 O Accepted, 2013; Perez Article 2

reactivity of specific proteins, the propensity sensorof and target proteins to interact to influencegeneto expression transcription factors must be modified for example by 2 . O 2 Redoxsensitive transcription factors and their target genes havenot been extensively studied O 2 synthesis during infection Pse potential H factors following H shows 2) increased sulfenylation proteins,of including protein sulfenylation using pulldowna Yap1 system or a ch al.et in

2 to actasto a

oxidises specific cysteineresidues and that isthere route a to reduce oxidised cysteines or this contextis - u

located 2 et al. domonas syringae , 2006) - Salamo , 2014; Bourdais 2 n effective O . GPX - - rich receptor 2 - Cys

like proteins, which arepotential sensors sensors. sensors.

et al. contradictory regarding the cytosolic interaction GPXL3of with ABI2 L P 2 s could also actas sensors lipidof hydroperoxides. Detection of increased O 2 rx O 2 , 2014) . The disulfide. The form binds to 2

2 responses,dependent is OXI1 on l signal, there mustbe specificity and thiscould be generated by the

challenge

has been detected andhave may a functional roleinhibiting IAA Recently, sulfenylation tryptophanof synthetase during response to

et al.et (Yuan - like kinases (CRKs) localised on the plasma membrane 2 2 . However,it should inborne be mind thatthe inductionHSP O O ht. All rightsht. All reserved. 2 2

, 2015; Lu . signalling

et al.et H (Waszczak

(Attacha Currently, is nothere biochemical detail butit is assumed 2 O 2

, 2017) activation of MAP kinases (MPK3 andpreviously 6), also

et al.et e.g. nd pathogen resistance.is It inducedH by

etal.

etal. modified .

(Kovacs , 2016; Kimura 2 O , 2017) , 2014; Akter 2

concentration gradients can form - Cys 2 O

et al.et by 2 . Modeling and the use HyPerof

thiol peroxidasethiol (Rentel 2 andshock heat transcription fact P O are present in various cellular gluthionylat rx 2 . Apoplastic H , 2016) emical trap for sulfenic acid(DYn

promoter

2 et al.et O

et al.et (Miller & Mittler, 2006; Jung

etal. 2

production and sensors. .

, 2017) oxidation , 2015)

, 2004) ion

(Shaikhali

responsiveness aof and transcription

2 and S O .

This would be indicating 2 . Ultimately, for

sensing may be

(Jacques - nitrosylat

et al.et

( Fig. 2

(Warren O , 2008)

(Miao et al. 2

3 and ion ors )

, et .

. -

This article isprotected bycopyrig inhibition and high light (Bonifacio undersome conditions theseare more resistant to oxidative stress, consistent with acclimation related stresses.Various studies APX with and catalasemutants, oxidation, we must supposethat this resultsin acclimation to potentially toxicH SinceH suchhigh as lightand inducedH by repair processes. Morefocussed studies show do that APX and that inducea similar setof genes,including HSPs and glutathioneS conditions increaseH responses to pathogens, UV typesThe genesof most widely induced arediverse in function and are also associated with proposed butit is difficult to assesshow coherent they are overrange a of treatments and superoxide and hydrogen peroxide transcriptomedata have attempted to identify groups genes of with specificity for singletO Which2. genes are influ between chloroplastsand nuclei approach shows that 2 newof genetically subtleapproaches areneeded tounravel H may putH the twofold. Firstly, mutants control H plantsis problematic. Catalase mutants exemplify this point. They H expression specificco pollen tube growth doesnot cause cell death reactive oxygen formation inshank the of the tubewhile H al.et 017) 2 Accepted ArticleO plant 2 , 2015) responsive genes responsive the problem posed by mutantsthat is extrapolation to function in wild type

combined with identification redoxof modifications to candidatesensor/target proteins. 2 O s 2 2

O

2 mpartments to addressspatial specificity include

adapt to thesepe etal. changesgene expression and directly affectsthe function of specificproteins cysteine by O to 2 . In poppy po

2 and that 2

O chloroplasts so farso outsideits physiological range thatpathological effectsare observed. More 2 , 2016)

a nd these genesare also controlled by other conditions that causeincreased H - encoded probes to follow H 2 H extreme excess O . Specifically, H 2

O 2 (Gechev encedH by

llencell tubes, death inducedself by in ROS scavenging or producing enzymes production (which is verfied i 2

(Fahnenstich induced gene - rturbationsremodeling by B andradiation, C ozone andother toxic chemicals, implying that these H 2 temperature O .

et al. 2

causes changescauses ingeneexpression and cell death.danger The is responses 2 O ht. All rightsht. All reserved. 2 , 2002) O 2

and is there an acclimatory response? 2 et al.et

expression pretreatment increased tobacco resistanceto catalase 2 s O

.

, 2008) (Mullineaux

2 (Wilkins (Willems Likewise,ascorbate deficient

2 sensing and signalling andlikely are to inv O 2

inand space time . While theseapproaches areuseful to identify is

et al.et facilitated by a closephysical association n some n some cases)or cause otherforms of damage

their et al.et

et al.et 2 , 2011) O redirection of transcriptome , 2016) 2 -

incompat the production atthe tip required for , 2018) thiol peroxidase

most recentlymost in suggest rice, that .Attempts at generating H show that catalaseis needed to may havepleiotropic effects - . Sets of transferaseslikely involved in

(Exposito .

i bility proteins involves glycolate oxidase . Secondly,the mutation vtc H 2 - O

Rodriguez mutants have higher M 2

2 expression is - O specificgenes are eta 2

exposureand - analyses of

olve et al.et tissues. 2 ,

2 the O ,

This and

2 2 O

in use 2

This article isprotected bycopyrig resolution. At the sametime, moreincisive physiological measurements modifications andnew by H in role cell wall biochemistry. This will beaided sensitive by detection of oxidative protein forward molecular genetics approach h and one theof signals for photosynthetic compared to non H Wherenext? IX. assess the actual benefit. universally beneficial and morestudies underrealistic environmental conditionsneeded are to this kind are contrary to thewidespread assumption thatincreasing antioxidant defences is H 2 2 AcceptedO Article O 2 2 2. stomatal

playsa prominent rolein plants,particularly becausephotosynthesis providesan extra source concentration

which plantsgrown in natural fluctuating conditions benefitfrom systemic signalli determine H ABA NOX signalling mediatedNOX by response was dependent onRBOHD a systemic rbohD H conditions influences gene expression inremoteleaves. involvement The of superoxide or and high lighthas beenproduced Sincethen further evidence for systemic signallin acclimation” was identified and proposed to be dependent H on well known. Systemic sign Systemic signalling we need betterto understandbiochemical the details of 2 2 O O 2 2

- (Dubiella via in transmiting the signal issuggestedattenuated by response of the NOX mutant mediated systemic acquired acclimationinteresting is and future workshould guard cells will continue to serveuseful as model systems. . Recently, a Ca stomatal closure -

photosynthetic organisms along withspecialised a ascorbate peroxidase. H

howit interacts with other potential signals (e.g. jasmonic acid)and the extent to and greater basal resistance pathogens to 2+

et al.et - dependent protein kinase,has been proposed, along involvement with of

it was shown that

. Systemic acquired resistance (SAR)in response to pathogen infection is , 2013b; Evans 2 O 2 as provided

probes ableprobes to providethe necessary ch alling high of lightresistance, termed “systemic acquired to the whole canopy ( - generated H

status and for stomatal movementsand ht. All rightsht. All reserved.

(Miller et al.et

a powerful means of identifying the a

local - mediated “ROS wave”. , 2016; Devireddy

2 et al. O

applicati 2

and activation Ca of , 2009) Devireddyal., et 2018 g inresponse to wounding, heat,cold, salt on on of . Exposure

(Mukherjee

high ligh

et al.et H 2 O 2 The possibleThe role of to cell cell

, 2018) and signallingwell as its as

emical, temporal and spatial

a target 2 2+ While than hitherto O t

channels and activation of stress et al.et 2

(Karpinski . Thepossibility of

). This systemic high light the dominant “ , 2010)

parts

leaf to the various can induce ”

, et al. are needed to . Results of t signalling o move ng. , 1999) a 2 O

2

is . This article isprotected bycopyrig AcceptedAwad J,Stotz HU,Fekete A,Krischke M,Engert C, Havaux M,BergerMueller S, MJ. 2015. AttachaSolbach S, D, Bela K,Moseler WagnerA, Schwarzlander S, M, Aller Muller I, SJ,Meyer AJ. ArthautL Arnaud Lee S, D, Takebayashi Y,Choi D, Choi J, Sakakibara Hwang H, I. 2017. Appenzeller Anjem A, Imlay JA. 2012. An Z, Almasalmeh KrencA, D,Wu B, Beitz E. 2014. S,Akter Huang J, Bodra N, De Smet B,Wahni K, Rombaut PauwelsD, J, GevaertCarroll K, Van K, References Articleinsightful comments. Michael J. Deeks contributed to our thinking includePhilip Mullineaux,M. colleagues whose hydrogen peroxidesignalling BiotechnologyThe and Biological Sciences Research Council provided funding for research on Acknowledgements attack may have a very differentphysiology, making translation to improvementcrop problematic. grown underfluctuating lightand temperature condit improves “stress resistance”. These effectsare revealed underlaboratory conditions while plants largenumber of studies assess the properties of mutants and transgenic plants. Aparticular concern isinterpretation of the

Jing W, Liu Y, Zhang W. 2008. Cysteineperoxiredoxins and thylakoid ascorbateperoxidase create a water membrane surfaces inArabidopsis thaliana. 2017. a consequence of the Ritz Klarsfeld T, A, etal. 2017. Arabidopsis. regulation reactiveof oxygen species homeostasis modula reticulum membraneis not sluggish. Kietzmann T, Laurindo F, Margittai E,etal. 2016. stress. Botany involved in abscisic acid permeability aquaporins.of Cellular& Proteomics BreusegemF, etal. 2015. - D,Jourdan Mteyrek N, ProcopioA, M, El -

Herzog C, Banhegyi G, Bogeski I,Davies KJ,Delaunay

Glutathione peroxidase Journal of Biological Chemistry

59 ,

Alistair M. Hetherington : : 815 important Plant Cell

-

825. (n

Mononuclear iron enzymesprimar are ot reviewed ot here)

contributions are not cited dueto lack of space. (BB/I020004/1

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Hydrogen peroxidegenerated by copper amine oxidaseis FEBS JournalFEBS ht. All rightsht. All reserved. - - -

like enzymes cover five distinctcell compartment - Blue 559. 2 basedIdentification of 1200.

cryptochrome photocycle.

and - lightinduced accumulation of reactive oxygenis species

and BB/N001311/1) in which over Free RadicalFree Biology and Medicine

Structural determinants of the hydrogen peroxide 287

Imogen Sparkes

281 : 15544 - Esawi M,D'Harlingue A, BouchetP PlantCell Environment & : 647 i ons alongons with exposurepest and pat Marino -

15556. - Transit of H - 656. expressing single antioxidantgenes Vicia faba

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tes stomataltes immunity in Apologies - Moisan A, Forman HJ, Gorlach A, PLoS OnePLoS 2 . O Journal ofExperimental 2

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oss oss the endoplasmic sulfenomes. are due : : 1281

Colleagueswho have 12 Cytokinin

94 : e0171836. : 157 - -- water , many 1295.

Murray Grant, -- - - s and E, Witczak J, mediated 160. Molecular cycle that

2 hogen -

This article isprotected bycopyrig AcceptedChaux F,Burlacot A, Mekhalfi M, Auroy P, Blangy S, Richaud Peltier P, G.2017. Bulleid NJ. 201 Buettner GR, Schafer FQ 2003. Bratt A, RosenwasserMeyer S, A,Fluhr R. 2016. Bourdais G, Burdiak P, Gauthier A, NitschSalojrvi L, J, RayapuramC, Idnheimo N, HunterK,Kimura BoronatS, Domenech A, PauloCalvo E, IA, Garcia Bonifacio A, Carvalho FEL, Martins MO, Lima Neto MC, CunhaRibeiro JR, CW, Margis Boisson Bodvard K, PeetersRoger K, Romanov F, N, Igbaria A,Welkenhuy ArticleBilan DS,Pase JoosenL, L, Gorokhovatsky AY, Ermakova YG, Gadella TWJ,Grabher C, Bienert GP,Heinen RB,Berny MC, ChaumontF. 2014. Bienert GP,Chaumont F. 2014. S,Bezzi Kessler D,Diezel C, Muck A,Anssour S, Baldwin IT. 2010. BerthetS, Demont Belousov VV,Fradkov AF, Lukyanov KA, Staroverov Shakhbazov DB, KS, TerskikhLukyanov AV, S. Bechtold U, Rabbani N, Mullineaux PM, Thornalley PJ. 2009. - 1825 promotefast and transient O Harbor Perspectivesin Biology 173 Vitamin C: Function Its and Biochemistry in Animals and Plants stress inCRKs responsesrelated to oxidativestress. S,Merilo E, systems. Barcons A, Serrano E, Carmonaal. M,et 2014. Journal ofPlant Physiology acclimation to copewith oxidative stressinduced by 3 Silveira JAG. 2016. via ANXURrece Nature communications Toledano Kall MB, M, etal. 2017. 542. performance for ratiometricand fluorescencelifetime imaging. Lukyanov S, Belousov VV. 2013. Biochimica Biophysica et Acta ZmPIP2;5, butnot ZmPIP1;2, facilitates transmembranediffusion hydrogenof peroxide. peroxide. from plantsin nature. increases nectar germin, nectarins, and hydrogen peroxidelevels and inhibits nectarremoval lignificationto of Balzergueet S, al. 2011. Methods 2006. 59 biomarkers for protein oxid Physiology is essential to protectthe photosynthetic apparatus underhigh lightstress conditions. Dernier A, Lituiev DS,Nestorova FranckA, CM,Thirugnanarajah S, Grossniklaus U. 2013. : 661 :

NADPH oxidases. -

188. –

. 1836. Genetically encoded fluorescent indicator for intracellular hydrogen peroxid 2. Plant,Cell and Environment - 671.

RedoxBiology 3 Disulfide bond formation inthe mammalian endoplasmic reticulum. Biochimica et Biophysica Acta

: 281 - 167

Caulet Pollet N, B, Bidzinski P, CezardLe L, Bris P, Borrega N, Herve J, Blondet E,

et al. 2015. ptor

: : 1592 - 286. - like kinasescoordinate cell wall integritywith growth atthe pollen tubetip Arabidop

Silenced ri

Plos BiologyPlos - 1603. PlantPhysiology

Ascorbate as anantioxidant. In:Asard H, May J, NSmirnoff eds. 2 Aquaporin

Large

8 Disruption of : 395 : : 14791. sis thalianasis

201 ation, nitrationation, and glycation inArabidopsis leaves.

2 ht. All rightsht. All reserved. - ce ince both cytosolicascorbate peroxidases displays pre

- scale phenomics identifies primaryand fine -

ph 399. 4

: : 17 Biomembranes : a013219.:

HyPer otoreduction in

11

- Light

-

facilitated transmembranediffusion of hydrogen 39 27. : e1001719.: : 1909:

LACCASE4 stems.

- 152 - 3: Agenetically encoded H sensing -

Organelle redoxautonomy during environmental General Subjects -

Santamarina S, Garcia : 2232 - 1919. PLoS Genetics Plant Cell

Maizepl

1838 Thiol

via and Chlamydomonas - 2242.

hydrogen peroxide andperoxiredoxin. a : 216 - based H

17

Quantitative measurementof specific - aminotriazole

asma membrane aquaporin 23

results in tissue -

222. : : 1124

Silencing NaTPI expression sen N, Palais G, Reiter W, 1840

11 2 O

. London: Taylor and Francis, : e1005373. 2 : 1596: ACS Chemical Biology -

signalling inmicrobial 1137. . P, Encinar Dedo Del J, 2 O PlantPhysiology - 2 inhibited catalase.

- probe with improved

1604.

- Flavodiiron proteins specific alterations -

tuning for roles

Cold Spring - Schultz C, Pinheiro M, PlantJournal e.

174 - Nature

8 Plant : : 535 :

-

This article isprotected bycopyrig AcceptedErmakova YG,Bilan DS, Matlashov ME,Mishina NM, Markvicheva KN,Subach OM,Subach FV, Engel Schmidt N, M, Lutz C,Feierabend 2006. J. Dubiella U,Seybold H,Durian G, Komander E, Lassig WitteR, CP, Schulze WX, Romeis T. Dubiella U,Seybold H,Durian G, Komander E, Lassig WitteR, CP, Schulze WX, Romeis T. 2013a. Drerup MM,Schlucking K, HashimotoManishankar K, P, Steinhorst KuchitsuL, K,Kudla 2013. J. Dietz K Devireddy AR, Zandalinas S DeLeon ER, Gao Y, Huang ArifE, M, Arora del Rio LA, Lopez ArticleDaudi A, Cheng Z,O'Brien JA, Mammarella Khan N, S,Ausubel FM, Bolwell GP. 2012. DatJF, Pellinen R, BeeckmanVan T, De Cotte B,Langebartels Kangasjärvi C, J, Inzé Van D, Costa A,Drago I, Behera S, Zottini M,Pizzo P,Schroeder Po JI, Corpas FJ,Pedrajas JR,Palma JM,Valderrama R, Rodriguez Consentino L, LambertS, Martino C, Jourdan N, BouchetP Claeys H, Van Landeghem S,Dubois M, Maleux K, Inzé D. 2014. Chen Chen D, Cao H, Y, Li Kim D, Ahsan N, Thelen J,Stacey G. 2017.

SX,Schopfer P. 1999. - J. 2016. for intracellularfor hydrogen peroxide. Bogeski I,Hoth M,Enikolopov G, etal. 2014. and properties lightof 8749. defensesignal propagation. Calcium Statesof America defensesignal propagation. Calcium kinaseCIPK26 regulate the Arabidopsis NADPH oxidaseRBOHF. CalcineurinThe B peroxidasesystems inthe photosynthesizing chloroplast? Signal overall stomatal response plants:of Rapid leaf physiology. Regulatory, integrative and comparative physiology identity: are reactive oxygen species actually reactive sulfidespecies? and CellPhysiology triggered immunity. apoplastic oxidative burst peroxidasein process intobacco. BreusegemF. 2003. Journal plantperoxisomes: an and response to oxidativestress conditions. JB. 2017. signaling mechanism. formation by CorbineauD'Harlingue F, A,etal. 2015. effects incommonly used peroxidase.of 2265. mediated RBOHD phosphorylation to regulatestomatal aperture.

11

62 - - Thiol dependentprotein kinase/NADPH oxidaseactivation circuitis required for rapid dependentprotein kinase/NADPH oxid

. - Immunological evidencefor the presence of peroxiredoxin in pealeaf peroxisomes

Huertas E. 2016. : 760: - Arabidopsis based peroxidasesand ascorbateperoxidases: plantsWhy rely European Journal ofBiochemistry - 772. -

110 like calcium sensors CBL1 and CBL9 together

57 Hydroxyl I, Gomez I, PlantJournal

Plant Cell Changesin hydrogen peroxide homeostasis trigger anactive cell death : 8744 New Phytologist : : 1364 - in vivo insensitiveplant catalases.

cryptochrome may definea novel evolutionarily conserved in vitro

ROS generation in peroxisomes androle its in cell signaling. - Proceedingsof the National Academyof Sciences Proceedingsof the National Academyof Sciences of the United – - - 8749.

radical production inphysiological reactions. Anovel function ht. All rightsht. All reserved. Cadenas A, Blumwald MittlerE, R. 2018. 1376. analysis uncoversa Ca

24

: : 275

33 stress assays.

N, N, Divietro A, PatelS,Olson KR. 2016.

: : 621 Nature Communications -

287. 206

Arabidopsis Blue Molecular identificat - 632. : 1450

Acta Physiologiae Plantarum -

lightdependent reactive oxygen species Red fluorescent genetically encoded indicator

- to ase activationase circuitis required for rapid Plant Physiology

260 - - 1462. leaf communication during lightstress. Plant,Cell and Environment -

- E,Witczak J,Castello El P, 2+ is a major component patternof : : 726 Ruiz M, ChakiM, -

dependent scavenging system.

zzan T, Lo Schiavo 2010. F. Extracellular ATP elicits DORN1

What is stress? Dose - Molecules and Cells 735.

5 ion, heterologous expression : 5222.:

with their interacting protein

Molecular Plant 310

165 Nature Communications : R549 : : 519

American journal of del Rio LA, Barroso

Coordinating the

- 39 A case of mistaken - 527. 560. : 57. on on multiple

- 110

- response

39

29 The Esawi M,

6

: 20: : 593 : 8744: : 559

2013b. H 2 O - - 25. Plant - 2 - - 607. Plant 569. in -

Sci

8

: This article isprotected bycopyrig AcceptedHarper AD,Stalnaker SH, Wells L, Darvill A, Thornburg R, York WS. 2010. Hara Hao Fan H, L, Chen T,Li R, He Li X, Gutscher M, Sobotta MC, Wabnitz GH, Ballikaya S, Meyer AJ, Samstag Y, Dick TP. 2009. Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz Samstag GH, MeyerY, AJ, Dick TP. 2008. Grondin A,Rodrigues Verdoucq O, Merlot L, S, LeonhardtN, Maurel C. 2015. GilroyBialasek S, M,Suzuki N, Gorecka M, Devireddy Karpinski AR, K,Gémes Kim YJ, ParkKY, Moschou PN, Gechev T,Gadjev I, V Gao Metz H, J, Teanby NA, Ward AD, Botchway SW, Coles B, Pollard MR, Sparkes I.2016. ArticleForeman J,Demidchik V,Bothwell JHF, Mylona Miedema P, Torres H, MA, Linstead Costa S, P, Ferreres F,Figueiredo R, BettencourtS, Carqueijeiro Oliveira I, J,Gil FarmerEE, Mueller MJ. 2013. Fahnenstich H, Scarpeci TE,Valle FlggeEM, U Exposito Exposito Evans MJ, Choi W - Chikuma M, Satooka Watanabe H, Honda S, T, Miyachi Y,Watanabe Verkman T, AS. 2015. Phytochemistry with a keratinocytes and development of psoriasis. Aquaporin cooperatively regulaterbohD dynamics and activity inArabidopsis. Chemistry based protein thiol oxidationH by time imaging of the intracellular glutathioneredox potential. 1945 ABA to Physiology calcium, and electric signals: Key mediators rapidof systemic signaling inplants. undersalinity. KA. 2016. Cellular and Molecular Life Sciences peroxide protects tobacco from oxidativestress inducing by set antioxidant a of enzymes. optical tweezers. quantification peroxisomeof tethering to chloroplasts intobacco epidermal cells using regulateplant cell growth. Brownlee C,Jones JDG, et al. 2003. vacuolar class III peroxidase: An H isolated vacuoles of the medicinal plant Valento Andrade P, PB, Duarte et P, al. 2011. Review ofPlant Biology system to study ox peroxide inchloroplasts of Arabidopsis overexpressing glycolate oxidaseas aninducible signall Photosynthesis Cadenas E, HyPer to examinespatial and temporal changes inH Plant Physiology AtRBOHD and TPC1 propagates thesystemic response to s - - Rodriguez M,Laissue PP, Yvon Rodriguez M,Laissue PP, Littlejohn GR, SmirnoffMullineaux N, PM 2013. - 1954. ing mechanism. fungal protein triggers a microbial surveillance and defense mechanism in nectar. - triggere

-

An NADPH - 284 G, GilroyMorris S, RJ. 2016.

171 3

Packer L eds. - mediated hydrogen peroxide transportis required for NF an BreusegemF, Inzé D, Dukiandjiev S, TonevaMinkov V, I. 2002. : : 31532 Plant Physiology : : 1606 -

d stomatal closure through OST1 dependent H 71

171 Plant Physiology : : 1963 idativestress. : : 1771 - - oxidase/polyamine oxidasefeedback loop controls oxidativeburst -

16015. ROS 31540. Nature Communications

64 - Methodsin Enzymology 1969.

: 429 - Q, Botella MA, Lin J. 2014. – Nature mediated lipid peroxidation and RES 1784.

2 ht. All rightsht. All reserved. O

- 2 172 450.

- transfer fromchloroplasts to nuclei providesa high Andronis E, Valassaki C, Roussis A, Roubelakis Plant Physiology Durocher G, Smirnoff N,Mullineaux PM. 2017.

2

2 422 170 O O : : 1418

59 Reactive oxygen species produced by NADPH oxidase 2 2

- affair? - scavenging peroxidases. : : 442 : 263 : 708: I,Maurino VG. 2008.

A ROS Catharanthus roseus - 1431. - - - 4 272. 714. Journal of E Nature Communications 46. -

assisted calcium wavedependent on Identification phenolicof compounds in

8

- : Article: number 49.

. Waltham, MA: Academic Press, mediated phosphorylation.

148 2 O

: 719 Clathrin and membranemicrodomains 2

in high light xperimental Botany alt stress inArabidopsis roots. - 729.

Generation of hydrogen S,Mittler R. 2016. - Nature Methods and theirinteraction with Iz Journal ofBiological quierdo PereiraA, DM, -

activated signaling.

Interaction Nectarinof 4 PlantCell - exposed plants.exposed In:

6

- Aquaporins contribute : : 7454.  B signalling in

62 The useThe of

PlantCell 26

5 : 2841

: : 553 : : 1729 ROS, -

Plant Angelakis

Hydrogen

Proximity

185

In vivo - Annual - light - 559. -

2854. - Real

201. 1745. 27 :

-

-

This article isprotected bycopyrig KarpinskiS, Reynolds H, Karpinska B,Wingsle G,Creissen G,Mullineaux PM. 1999. KärkönenDewhirst A, RA, Mackay CL, Fry SC. 2017. KadotaSklenar Y, J,Derbyshire P,Stransfeld L, Asai S,Ntoukakis Jones V, JDG,Shirasu Menke K, F, KadotaShirasu Y, K, Zipfel C. Jung H J JacquesGhesquiere S, B,De Bock PJ,Demol H, WahniWillems K, P,Messens J,Van BreusegemF, Izumi M, Ishida H, NakamuraHidema S, J. 2017. Iqbal A, Yabuta Y, Takeda T, NakanoShigeoka Y, 2006. S. Imlay JA. 2013. Imlay JA. 2008. Idänheimo N, Gauthier A, Salojärvi J,Siligato R, Brosché M,KollistH, Mähönen AP, Kangasjärvi J, HuangVan S, Aken Schwarzlander O, M, BeltMillar K, AH. 2016. HuangStein BK, KT,Sikes HD. 2016. HuangSikes BK, HD. 2014. HeupelMarkgraf R, T, Robinson DG, HeldtHW. 1991. HeupelHeldt R, HW. 1994. Hernández Acceptediménez A,Hernández JA, Rio LA, Sevilla F. 1997. Article - S,Crisp PA, Estavillo GM, Cole Hong B, Mockler F, TC, Pogson 654 signaling and acclimation in responseto excess excitation en wall. peroxidaseaction and inducenon KinaseBIK1 during Immunity.Plant Jonesetal. A, 2014. Plantand Cell Physiology 14474 light. heat 284. glutathione cyclein mitochondria and peroxisomes of pealeaves. oxidativestress. Gevaert K. 2015. to the central vacuole by autophagy. 5597. specificglutathione peroxidase isoenzymes of lessons from a model bacterium. Biochemistry Communications CRK7 protect againstapoplastic oxidativestress. Wrzaczek M. 2014. 1559. oxygen encoded tools to study its toxicity to human cells. concentration. devoid intact of b peroxisomes: evidencefor channeling photorespiratory of metabolites inperoxisomes 165 complexinvolved inphotorespirato theof Wu AY, HM, Cardenas L. 2015. - - Barrera VelardeA, -

172. 657. - Archivesof Biochemistry and Biophysics shocktranscription factors required for the early response of Proceedingsof the National Academyof Sciences oftheUnited States ofAmerica

- Arabidopsis 14479.

speciesin cellular signalingresponse and stress in plants. The molecular mechanisms and physiological consequences of oxidative stress: Cellular defensesagainst superoxideand hydrogen peroxide.

77

RedoxBiology : 755 Molecular Cellular& Proteomics

445 Protein methionine sulfoxidedynamics in oundary membrane. root elongation zone to aluminum treatment.

Quantifying intracellular hydrogen peroxide perturbations interms of

Protein organization inthe matrix leafof peroxisomes: A multi‐enzyme The

Direct Regulation of the - : : 457 2015. 776. - Buendia A, ZepedaSanchez I, Quinto F, C,Sanchez Arabidopsisthaliana

56 - 462.

Regulation of the NADPH oxidaseRBOHD during plantimmunity. : : 1472

Modulating and measuring intracellular H ht. All rightsht. All reserved. 2

: : 955

HyPer,a hydrogen pe Nature Reviews. Microbiology - - enzymicH 1480. ry metabolism. Molecular Cell - 962. PlantCell Plant Physiology

Entirephotodamaged chloroplastsare transported

Evidencefor thepresence of theascorbate

Metabolites 2,3of

2

cysteine NADPH OxidaseRBOHD by thePRR 620 O

Arabidopsisthaliana

Compartmentation studies spinachon leaf 29 2 generation: Potential roles in the plantcell

Biochemical and Biophysical Research : 12: 14 : : 377

ACS Synthetic Biology Hydroperoxidereduction by 54 European Journal ofBiochemistry : 1217: - : : 43 roxide sensor, indicatesthe sensitivity -

22. rich recep -

394. 96 --

The roles of mitochondrial reactive : : 971 - 55. 1229. Arabidopsis thaliana

ergy inergy

BJ, Chory2013. J. - -

diketogulonate delay 979. 11 tor

Sensors Plant Physiology Plant Physiology : 443 Arabidopsis . - Arabidopsis likekinases CRK6 and FEBS JournalFEBS

Annualof Review 2 O --

5

454. 2 15 : 1389

using genetically - Lopez R,Cheung : : 855

Systemic

thioredoxin to excess . -

Subset of 1395. - under -

Science Associated 273 867.

171

114

- : 5589 220

: 1551

: 275 110

284 : : - - - - : This article isprotected bycopyrig AcceptedLaitinen Morreel T, K, Delhomme N, Gauthier SchiffthalerA, B, Nickolov K, Brader G, LimK Kristiansen KA, Jensen PE, Mller SchulzIM, A. 2009. Kovacs I, Holzm Koo Kobayashi M,Ohura Kawakita I, K, Yokota N,Fujiwara M,ShimamotoDoke K, N, Yoshioka H. 2007. KneeshawKeyani S, DelormeR, Kleff S,Sander Mielke S, G,Eising R. 1997. Kitajima S, Nii H,Kitamura 2010. M. KimuraWaszczak S, Hunter C, K,Wrzaczek M. 2017. ArticleKimuraKaya S, Kawarazaki H, T, Hiraoka G, SenzakiE, Michikawa M, Kuchitsu K. 2012. Kimura M, Umemoto KawanoY, T.2014. Kim Khokon Kaya H, Nakajima R, Iwano M,Ka Kaya H, Nakajima R, Iwano M,Kanaoka MM,Kimura S,Takeda Kawano 2003. T. JC, LeeJC,Dai IC, C,Lee Y,Cho HK, Kim Y, Phee BK, H,Kim Lee IH, Choi SH, et al. 2017. HJ, Kato N, Kim S, Triplett B. 2008.

metabolism. Street TH, NR, etal. 2017. laser microscopy. and localisation inliving cellsuse by offluorescent the CM probe Science reductase contributes to theactivation anti of Linster E, Hell R,Arnold GJ,etal. 2016. cell death inArabidopsis. RPK1trio Potato NADPH Oxidase. Calcium Natl Acad Sc 2017. peroxisoma sunflower cotyledons iscatalase a that differs inprimarystructure from thecatalase inthe Biochemistry showed improved toleranceto hydrogen peroxide. species inreceptor reactive oxygen species. oxidases and function may triggeras a forpositive the feedbackregulation of Ca phosphorylation isprerequisite a for the Ca stimulus. by plantpero evidencefor anextracellular form. production in Arabidopsis. induced stomatal closureaccompanied by peroxidase 1069 by Arabidopsis RbohH and RbohJessential is for proper pollen tubetip growth. Hamamura Y, Higashiyama T, etal. 2014. 1069 by Arabidopsis RbohH and RbohJessential is for proper pollen tubetip growth. Hamamura Y, Higashiyama T, etal. 2014. defenseand growth induction. MAR, UrajiMAR, M, MunemasaOkuma S, E, Nakamura Y, Mori MurataIC, Y. 2010. - --

1080. Nucleoredoxin guards against oxidativestress by protecting antioxidantenzymes. 1080.

eister Wirtz C, M, Geerlof A, Frohlich T, Romling G, Kuruthukulangarakoola GT, 7 - Dependent Protein Kinases Regulate the Production Reactiveof Oxygen Species by

: : 1669. - Roles of thereactive oxygen species Frontiersin Plant Science CaM4

l matrix.

i U A S

Plant Physiology xidase: hypotheses and supportivedata employing ferrous ion as a model 74 - : 1501

RbohF mediatestransient superoxide production to trigger age Physiologia Plantarum . -

likekinase signaling. European Journal ofBiochemistry - 1503. - the Plant Cell Online Biochimica biophysica et acta Hinoux V,Imrie L,Loake Le GJ, Bihan T,Reichheld Spoel JP, SH. Cell Reports naoka MM,Kimura S,Takeda Kawarazaki S, T, Senzaki E,

A key rolefor apoplastic H Bioscience, Biotechnology, and Biochemistry

Recombinantstromal APXdefective in the unique regionloop ht. All rightsht. All reserved. 174 Plant CellReports

Cu/Zn superoxidedismutases in developing fibers: cotton

: : 1449 Hydrogen peroxide

Planta 5 Thepredominant protein inperoxisomal cores of : : 285.

21

- ROS

: : 3373 Plant Cell 1475. 136

228 Ca Ca 2+ -

: : 369 mediated inhibition S of 2+ 2+ Monitoring reactive oxygen species formation - 19 Boundfate: by role The of reactiveoxygen - dependent activation Arabidopsisof NADPH : : 281 - generating peroxidase reactions inplant

- - oxidativemechanisms. - activated reactive oxygen species production activated reactive oxygen species production 3380. : 1065:

21 -

383. 29 - Bioscience, Biotechnology, and 292. : 829 : 638

2 -

- --

O independent generation superoxideof

mediated reactive oxygen species 245 1823

1080. 2

S,Kawarazaki T, Senzaki E, - in Norway spruce phenolic 837. - : 402 654. : : 398

- 410. - - 405. H 2 DCFDA and confocal

- nitrosoglutathione

Frontiersin Pla

74 : 2313

Chitosan PlantCell PlantCell -

2+ Protein

- dependent Theprotein 2315.

and - J, Teeri nt

- Proc

26 26 : :

This article isprotected bycopyrig AcceptedMelo EP, Lopes C, Gollwitzer P, LortzLenzen S, Mehmeti S, Kaminski I, CF,Ron AvezovD, E. 2017. MatsusakiM, OkudaMasuda A, Koishihara T, Mita K, R, Iwasaki K, Hara K, NaruoHirose Y, A, Matlashov ME, Bogdanova YA MarutaSawa T, ShigeokaY, Ishikawa S, T. 2016. MarjamaaKukkola K, EM, FagerstedtKV. 2009. Marinho HS,Real C, Cyrne SoaL, ManganoDenita S, LuLiang K, Wu S, Z, Bi C, Yu YT, Wang XF,Zhang DP. 2016. JB, Lim Barker KA, Huang BK,Sikes HD. 2014. ArticleLiang Ding X, P, LianWang K, J,Ma M, Li L L, Li X, Imlay JA. 2018. L,Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L,Zhang X, Wang Y,etal. 2014. J, Li Liu J,Wang G,Cha J Levine Mosoni RL, L, BerlettStadtmanBS, ER. 1996. Lee Y, Rubio MC, Alassimone J,G Le D Laugier E, Tarrago L, eunff Davoine E, C,Le Dantec C,Billard JP, HuaultC. 2004. BMC BiologyBMC TriPer, an probeoptical tuned tothe endoplasmic reticulum trackschanges inluminal H oxidoreductasesand ERO1 in soybean. Tsuchi Y,etal. 2016. Acta SypHer2: Applications inneuroscienceand regenerativebiology. OkabeLukyanov S, Enikolopov S, G, etal. 2015. Physiology functions inchloroplasts: morethan a just classical antioxidant enzyme? lignification. regulation transcriptionof factors. America polar growth. Barberini ML, Aptekmann AA, etal. 2017. confers drought tolerance. cysteine Journal ofMicrobiological Methods HyPer,probe a for hydrogen peroxide,in bacteria exposed to external oxidative stress. 5 heterotrimericproteins G regulateimmunity by directlycoupling to the FLS2receptor. 217 defineits threshold of toxicity for immunity. associated kinaseBIK1 directly phosphorylates the NADPH oxidaseRbohD to control plant responstress function NOCATALASE of ACTIVITY1 required is to maintain catalaseactivity and for multiple Statesof America antioxidants inproteins. endodermis. leaf sheaths. germin/oxo reductase capacity and growth underhigh light. 2013. : : e13568. - 227. -

Involvement of thioredoxin y2 inthepreservation of leaf methionine sulfoxide General Sub - 114

rich receptor

Cell Host Microbe 57 -

Juarez SP, Choi H genes during wounding ryegrass of blades: leaf comparison with senescence of

: 5289 Improved measurements of scanthydrogen peroxide enableexperiments that

Journal ofExperimental B Courteille A, Innocenti G,Eymery F, Rumeau D, Issakidis Cell PlantJournal 15 sesin Arabidopsis. : 1377 Proceedings of theNational Academyof Sciencesof the United Statesof : : 24. -

Y, Li G, ChenLi S, Z, Guo J,Zhang C, Yang etY, al. 2015. 153

93 jects - 5294. -

: : 15036 1386.

: 402 : Cooperativeprotein folding by two protein thiol disulfide - , Ermakova MishinaGV, Ermakova NM, YG, Nikitin ES,Balaban PM, like protein kinase, CRK5, enhances abscisic acidsensitivity and

1850 Proceedingsof theNational Academyof Science res H,res Antunes F. 2014. eldner N. 2013. -

38 412. Journal ofExperimental Botany -

: : 2318 15040. 1 : 421 : ht. All rightsht. All reserved. - 5 S, Marzol E, Hwang Y, Ranocha P

: : 329 PlantCell Escherichia coli - - Redox Biology 431.

2328.

106 - i L,i Li M, Zhang X, Chenet S,al. 2016. 338.

In otany Plant Physiology

: 33

- The role of xylem class III peroxidasesin

depth characterization of the fluorescent signal of

Diversityand evolution of ascorbate peroxidase

A mechanism for localized lignin deposition inthe 27

Molecular linkbetween auxin and ROS - 39.

60 : : 908 Methionineresidues as endogenous : 367:

Plant, Celland Environment

Fluorescent ratiometric pH indicator

. Hydrogen peroxidesensing, signaling and 2 - Free Radical Biology and Medicine 925.

: 535 : Overex - 376.

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pression anof Arabidopsis

67 :

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This article isprotected bycopyrig AcceptedNakamura J,Purvis ER, Swenberg JA. 2003. Nagano M, Ishikawa T,Fujiwara M,Fukao Y,Kawano KawaiY, MyougaHosoda F, C,Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi Mullineaux PM,Exposito Muller SchneiderA, JF,Degrossoli A, Lupilova N,Dick TP, Leichert LI. 2017. Mukherjee M,Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB,Barth C. 2010. Mueller S. 2000. Mubarakshina Borisova MM,Kozule Morris JJ,Johnson Szul ZI, MJ,Keller M, Zinser ER. 2011. ArticleMorgan MJ,Lehmann M,Schwarzlander M, Baxter CJ,Sienk Morgan B, Mitsuya S, El Miller G,Schlauch K, Tam R, Cortes D, Torres MA,Shulaev Dangl V, JL,Mittler R. 2009. Miller G,Mittler R. 2006. MiaoLv D, Y, Wang WangP, X Messner KR,Imlay JA. 2002. Membré N, Bernier F,Staiger D, Berna Nucleic oxidative DNA lesions moreefficiently than millimolar concentrations in mammalian cells. rice. Plasma membrane microdomains are essential for Rac Arabidopsis nucl M,Shinozaki K. 2008. Radical Biology and Medicine pathways inplantsand algaeexposed to high light: RadicFree Biol Med assessment of 23 hydrogen peroxide,salicylic acid, and the Ascorbic acid deficiency in systems. chloroplastenvelope aquaporins.via Photosyntheticelectron flowto oxygen and diffusion hydrogenof peroxidethrough the surface. Prochlorococcus hydrogenon peroxidescavenging microbes for growth at the ocean's and mitochondrial redoxhomeostasis. superoxide dismutaseleads to reduced growthroot and affects tricarboxylicacid cycleflux SchauerFernie N, AR, Fricker MD, Ratcliffe RG,etal. 2008. Chemical Biology 2016. NaCl tolerancein peroxisomecauses proliferation, butinducing peroxisomeproliferation doesnot improve Science Signaling NADPH oxidaseRBOHD mediatesrapid systemic signaling inresponse to diverse stimuli. sensors in droughtstress responses. peroxidasefunctions as both aredox transducerand a scavengerin abscisic acid and Chemistry fumaratereductase, succinate deh and specificfeatures point ato variety of functions. : 340 : Van LaerOwusu K, Ezerina TN, D, Pastor eoids againsteoids oxidative stress and is essential for chloroplast development in Plant Cell -

Shami M,Sparkes IA, CharltonLousa WL, Cde M,Johnson B,Baker A. 2010. Real

- AcidsResearch 351. PLoS One

Sensitive Free Radical Biology and Medicine

- 277 plants? time monitoring basal H2O2 of levels with peroxiredoxin .

Plant Cell

: : 42563 responses of roGFP2 28

: : 1966

-

2 Arabidopsisthaliana

Could heat shocktranscription factors function as hydrogen peroxide 12 Rodriguez M, Laissue PP, Smirnoff N. 2018. 6 Annals of Botany and nonenzymatic measurement hydrogenof peroxidein biological : ra45.: : : e16805.

106

: 437 : Mechanism of superoxideand hydrogen peroxide formation by -

A heterocomplexof iron superoxidedismutases defends chloroplast 42571.

- 20 31 C, C, Chen J,Miao C,Song C - : 329 : 1983.

: : 3148 - : : 1790 PlantCell 443. Arabidopsis

va MA, Rudenko NN, Naydov Klenina IA, IB,Ivanov BN. 2012. - . ht. All rightsht. All reserved. 338.

- A. 2000. - 3162. 1795.

ydrogenase,and aspartate oxidase.

-

98 18 based probes to physiologically relevant oxidantspecies. Micromolar concentrations hydrogenof peroxideinduce Biochimica et biophysica acta

.

: 279

: 2749 Plant Physi induces c PLoS OnePLoS

Arabidopsisthaliana NPR1 -

29 288. - - Flores D,Amponsah PS, Tursch DickA, TP. 2766. : 410 gene. onstitutivepriming thatdependent is on

-

5 Dependence theof cyanobacterium P. 2006. ology : e9408.:

- Comparisons with other eukaryotes. Planta 415. iewicz

Molecular Plant 1 -

- Yamada M,Shimamoto 2016. K. 147 RbohB/H

An

211 -

: : 101 Decrease in manganese Porzucek A, Williams TCR,

germin Arabidopsis

ROS : 345 - 114. - mediated immunity in -

1817 dependent signalling

- - Systematic invitro 354. based probes. - like proteins: common -

Microbe Interactions Journal of Biological : : 1314

glutathione - 1321.

The plant

Salt stress Nature

Free

This article isprotected bycopyrig AcceptedQueval G, J,WangQi J, Gong Z, Zhou JM. 2017. Price NJ,Pinheiro C,Soares CM, Ashford DA,Ricardo Jackson CP, PA. 2003. PotockyM, Pejchar P, Gutkowska M,Jimenez Poole B. 1975. Polle A,Junkermann W. 1994. Pilon M, Ravet K, Tapken 2011. W. Perez Peiffer M, Tooker JF, Luthe DS,Felton GW. 2009. Orman Ogasawara KayaY, H, HiraokaYumoto G, Kimura F, S,Kadota Hishinuma Y, H ArticleNoctor G,Mhamdi FoyerA, CH. 2016. Nguyen Navrot N,Collin V, Gualberto J,Gelhaye E,Hirasawa M,Rey Knaff P, DB, Issakidis E,Jacquot J Nauser Koppenol T, WH. 2002. NarendraVenkataramani S, Shen S, G, Wang J,PasapulaLin V, KornyeyevY, D, Holaday AS, Zhang Nakashima K, Fujita Y,Kanamori Katagiri N, Umezawa T, T,Kidokoro Maruyama S, K,Yoshida T, - Salamo I,Papdi C, Rigo G, ZsigmondVilela L, B, Lumbreras V,Nagy I,Horvath B, DomokiM, - Ligeza Parizot B, B, de Rycke R,Fernandez A, HimschootEa. 20 - Arabidopsis photorespiratory mutant Maslow M, Van BreusegemF, Noctor G. 2007. PlantBiology Chemistry molec phospholipids and Rac/Rop GTPases. V. 2012. Jou 617 Norway spruce by the photooxidanthydroxymethyl hydroperoxide. superoxide dismutases. Physiology oxidativestress and the mitogen Darula et Z, al. 2014. sensors for insect herbivores. production facilitateslateral root emergencein Arabidopsis. Ca S,Nagata K, etal. 2008. successful data collection and interpretation. sequences. peptideligand library and description unexpectedof Hyp inperoxidase amino acid thaliana Physiology several subcellular compartmentsand regulated during and biotic abiotic stresses. Rouhier N. 2006. 4086. monoxide: Experimental Botany antioxidant enzymeand is dispensable for 2006.H. 1345 Essential for the Control of Seed Development and Dormancy. SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, Ishiyama K, Kobayashi M, etal. 2009. Kim H,Kim San Clemente H, Balliau T,Zivy 2+ Issakidis rnal ofTheoretical Biology -

621. and phosphorylation. -

1363. ular characterization LEP1,of an extensin peroxidasefrom lupin.

Diffusion effects in the metabolism hydrogenof peroxideby liver rat peroxisomes.

root cell wallproteomics: Increasingproteome the coverageusing combinatorial a

NADPH oxidaseactivity inpollen tubesaffected is by calcium ions, signaling The

278

- 165 142

Proteomics Bourguet HoeberichtsE, FA,Vandorpe M,Gakiere B,Vanacker Miginiac H, Approaching thediffusion limit.

Arabidopsis 38 : : 41389 : : 319 : 1364 : 92:

Plant glutathionePlant peroxidases are functional peroxiredoxins distributed in - - 334. 100.

-- 57 Theshock heat factor A4A confers salt toleranceand is regulated by - 41399.

1379.

Inhi

16 The rateThe constant theof reaction superoxideof with nitrogen : : 3033 Biochimica Biophysica et Acta

Synergisticactivation of the Arabidopsis NADPH oxidase byAtrbohD

ascor : 491 Journal ofBiological Chemistry bition apoplasticof and symplasticperoxidase activity from

The biogenesisThe and physiological function of chloroplast

ht. All rightsht. All reserved.

Apoplastic ROS signaling inplantimmunity. New Phytologist 51 -

Oxidativestress and antioxidativesystems: Recipesfor 3042. bateperoxidase 3 a is peroxisomal membrane - 5 : 149: - 03. activated protein kinase

Journal of Plant Physiology - cat2

167. - Three Arabidopsis SnRK2 Protein Kinases, Quesada MJ,Potocka A, Alche Jde Kost D, B, Zarsky

M, DunandAlbenne C, C,Jamet E. 2016.

Plants on early alert: Glandular trichomes as

Arabidopsis

demonstratethat redox state iskey a modula The Journal ofPhysical Chemistry A Plant,Cell and Environment

184

Conditional oxidative stress responsesin the : 644

- growth and development.

-- Bioenergetics 656.

s MPK3 and MPK6. 283 Involved in ABA Signaling are Development

: : 8885 Plant and Cell Physiology 16.

169

RBOH - Plant Physiology : : 1654 8892. A biochemical and

1807 , Senzaki, E, Yamagoe Journal of Biological - : : 1140 CurrentOpinion in mediated ROS : dev.136465.:

: 989 : - 1663. Plant - bound

- - 106 1160. 998.

Arabidopsis Journal of Plant : 4084:

104

- P

-

50 tor : , - : This article isprotected bycopyrig AcceptedShimakawa G,Ishizaki K, TsukamotoTanaka S, M,Sejima Miyake T, C. 2017. Shigeto J,Itoh Y, Hirao S, OhiraFujita K, K,Tsutsumi Y. 2015. Shibata M,Oikawa K, YoshimotoKondo K, M,ManoYamada S, Hayashi K, M,Sakamoto W, Shaikhali J,Heiber I,Seidel T, Stroher E,Hiltscher H, BirkmannDietz S, K Semchyshyn HM, Valishkevych BV. 2016. Segal AW. 2016. Seaver LC,Imlay JA. 2001. ScuffiD, Nietzel FinoT, Di Meyer L, AJ, LamattinaSchwarzlander L, M, Laxalt AM,Garcia Schwarzlander M,Fricker MD, Sweetlove LJ. 2009. Schwarzlander M,Fricker MD, Muller C,Marty L, Brach T, Novak J,Sweetlove LJ,Hell R ArticleSchmitt FJ,Renger Friedrich G, T,Kreslavski VD, Zharmukhamedov SK,Los DA, Kuznetsov VV, Ruff Rodríguez Rodrigues O, Reshetnyak G, Grondin SaijA, Riemer J,Schwarzlander M,Conrad M,Herrmann JM. 2015. Richards SL, Wilkins KA, Swarbreck SM,Anderson AA, Habib N, SmithMcAinsh AG, M, Davies JM. RentelMC, Lecourieux D, OuakedUsher SL, F, PetersenOkamoto L, H, Knight H,Peck SC, Grierson er M,Steipe B, Zenk MH. 1995. Phy Marchantia, drives alternative electron flow usingflavodiiron a protein to protect PSI. Integrative Plant Biology AtPrx25 autophagy in Ohsumi Y, Nishimura M. 2013. peroxiredoxin A and other chloroplastantioxidant enzymes. redox Involvement of TOR and glutathionereductase. fungi, plantsand humans. Escherichia coli Physiology peroxide and phospholipaseD 2018. oxidative challenge. mitochondria: Effect respiratoryof in Microscopy 2008. Bioenergetics and in role stress Allakhverdiev SI. 2014. catalase. mediated induction of the peroxin PEX11a. Peroxisomes extend peroxules inafastresponse to stress the United Statesof America pathogen Aquaporins facilitatehydrogen peroxideentry into guard to cells mediate ABA operation and physiological relevance. 37 2015. Arabidopsis HirtCS, etal. H, 2004. regulation H of daylengthof - - Serrano M,Romero 46. siology

- Hydrogen sulfid Confocal imaging of glutathioneredox potential inliving plantcells. The hydroxyl radical in plants

sensitivetranscription fac

and NADPH oxidasesas electrochemical generators to produceion fluxes and turgor in FEBS Letters - triggered stomatal closure.

10.1104/pp.17.01636 173

. 231 - AtPrx71 Nature dependent geneexpression, and define photoperiod ascrucial a factor in the

Arabidopsis 1837 : : 1636 2 . : 299 O Journal of Bacteriology - 2 signaling inphototrophic organisms. -

Hydrogen peroxidefluxes and compartmentalization in induced death. cell : 835

427 BiochimicaBiophysica Et Acta -

- alters lignin content and structurein 316.

1647. e increasesproduction NADPHof oxidase 377

OXI1 kinaseis necessary for oxidativeburst -

Puertas MC,Sanz Reactiveoxy - : : 858

848. 57 .

: 175 Open Biology PlantCell

: : 349

Evidence againstspecific binding salicylic of acid to plant

-

114 ht. All rightsht. All reserved. 861. - -

derived phosphatidic acid inguard signaling. cell 180. Highly oxi tor Rap2.4a controls nuclear expression of 2 - : : 9200 . 356.

Hormetic effect H of : from: seed to seed.

o Y, LeonhardtN, Maurel C,Verdoucq L. 2017. 25 gen species: Re hibitors, abiotic stress and assessment recoveryof from

Proceedingsof the National Academyof Sciencesof Plant Journal : : 4967 Biol Chem –

183 6 9205 9205 dized peroxisomesare selectively degraded - : 160028. Fernández M,HuJ,Sandalio LM. 2016.

PlantPhysiology : : 7182 Monitoring the invivo redoxstate plantof - 4983.

Dose

396 - - 7189.

Bioenergetics

- 52 evaluation of generation, monitoring

- : 465 Thiol switches in mitochondria:

Response Simultaneouslydisrupting : : 640 2 Biochimica Biophysica et Acta O Journal ofExperimental Botany

2

via - Arabidopsis in 482. -

657. 171 BMC PlantBiology Saccharomyces cerevisiae

a reactive oxygen species

-

14 dependent hydrogen : : 1665

1787 - J, Baier M. 2008. - : : 1 mediated signalling in - 12.

: 468 The liverwort,

- stem. 1674.

sidegrowing Journal of - 475. -

Journal of Cys -

8 and

Plant , Meyer, AJ. AtPrx2, : 48.

- Mata C.

The -

via

Plant : - 66

: This article isprotected bycopyrig AcceptedWillems MhamdiP, A, StaelStorme S, V,Kerchev P, Noctor G,Gevaert K, Van BreusegemF. 2016. Willekens H, ChamnongpolDavey S, M,Schraudner M,Langebartels C,Van Montagu M,Inzé D, Wilkins KA,Bancroft J, Bosch M, Ings J,Smirnoff Franklin N, Wheeler G, Ishikawa T, Pornsaks Waszczak C,Akter S, Eeckhout PersiauD, Wahni G, K, Bodra Na. 2014. Warren EAK, Netterfield TS,Sarkar Kemp S, ML,Payne CK. 2015. Veredas FJ,Canton FR, Aledo 2017. JC. Van Raamsdonk JM,Hekimi S. 2009. TianWang S, X, Li P, Wang Ji H, H, J,Xie QiuQ,Shen DongD, H. 2016. Tavladoraki P, Cona A, Angelini R. 2016. TaubertD. 2003. ArticleTattini M, LoretoFini F, A, Guidi L, Brunetti TakedaGapper S, C,Kaya BellH, Kuchitsu E, Dolan K, L. 2008. Sweetlove LJ, LytovchenkoMorgan A, M, Nunes SundaravelpandianChandrika K, NNP, SchmidtW. 2013. SultanaFlorance N, HV,JohnsSmirnoff A, N. 2015. StrandLivingston DD, AK, Satoh Šnyrychová I, A Sirichandra C, Gu D,Hu HC,Davanture M,Lee S, Djaoui M,Valot B, Zivy M,Leung J,MerlotS, et al. The ROSThe Wheel: refining ROS transcriptional footprints. plants. Van C incompatibility response of species and nitric oxide mediateactin reorganization and programmed cell death inself the 4:e06369. pathways for vitamin C following plastid acquisition inphotosynthetic eukaryotes. of America Arabidopsisthaliana sensing hydrogen of peroxidein living cells. preferentially oxidized extends lifespan in 1650. linksapoplastic H Frontiersin PlantScience polyamine oxidasesare key players inplant Radical Biology and Medicine 613 stressed phenylpropanoidspart are theof antioxidantdefense orchestrated dailyby drought determines cell shapehair inroot cells. 19587 Proceedings ofthe National Academyof Sciencesof t AR. 2006. in Arabidopsis. subunit, controls roothair differentiation through reactive oxygen species(ROS) distribution glycoproteome in Sciencesof the United Statesof America cyclic electron flowby hydr comparison of methods. FebsLetters 2009. - 626.

amp W. 1997. Phosphorylation theof Arabidopsis AtrbohF NADPH oxidaseby OST1 protein kinase. - 19592. EMBO Journal yaydin F, Hideg E. 2009.

Platanus acerifolia ×

R

Mitochondrial uncoupling proteinrequired is for efficientphotosynthesis.

eaction constantsrate superoxideof scavenging plant by antioxidants. 111

583

: 11545: New Ph : 2982 2 O Arabidopsisthalia

Caenorhabditiselegans 2

.

Catalaseis a sink for H induction to diseaseimmunity pathways.

Proceedingsof theNational Academyof Sciencesof the United States 16 - - ytologist in vivo 2986. 11550. - : 4806

Physiologia Plantarum Cruz M,FroehlichCruz Maurino JE, VG,Kramer DM. 2015. itV,Smirnoff N. 2015. 7 : 824. ogen peroxideogen Papaver

ht. All rightsht. All reserved. Deletion theof mitochondrial superoxide dismutase sod plantsduring Mediterranean summers. 35 understress conditions.

-

4816.

Methionine residuesaround phosphoryla

197

: : 1599 Detecting hydrogen peroxide inleaves in vivo

Copper

: : 151 . na C,Velikova Gori V, A,Ferrini F. 2015.

Plant Physiology - . 1607. Science Plant, Celland Environment

- 112 - - containing amine oxidases and FAD 161. Nesi A, Taylor NL, Baxter EickmeierCJ, Fernie I, in vivo . 2

O PLoS Genetics Scientific Re tissuedifferentiation and organ development. Ascorbatedeficiency influencesthe leaf cell wall : 5539

2

andindispensable is for stress defencein C

319

135 Evolution of alternative biosynthetic .

Proceedingsof the National Academyof PFT1, a transcriptional Mediator complex – : : 1241 : : 1 5544. - he United Statesof America Tong VE. 2011.

156 -

Scientific Reports Local positivefeedback regulation 18. ports Plant Physiology

- : : 404

Spatially 5 1244. : : e1000361.

5

: : 16929. Plant Physiology - Plant aquaporinPlant AtPIP1;4

416. Sulfenomemining in

- resolved intracellular

38

Reactive oxygen New Phytologist : 375

7

171 tion sitestion are : 40403.:

Isoprenoids and - 384. - : : 1720 dependent -

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103

Free eLife - : 1635: 1733. - :

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- This article isprotected bycopyrig Acceptedcompounds tested quercetin, gallicacid, epicatechin gallate and oligomericproanthocyanidins were determined by hydroxyl groups: reactivity of phenolic compounds (e.g. cinnamic acid derivatives and flavonoids)is largely 20at Conditions for rate constantdetermination aredescribed inreferences the butare usually pH 7 Table 1 yr c Zou J Zipor G, Zhang Z, Xu Y, Xie Z, Li X,He Z Zhang Y, Zhu Zhang H, Q, Li M, Yan M,Wang WangR, Welti L, R, ZhangWang W, X. 2009. ArticleZhang Y, DingLu S, Q, Yang Z, Wen X, Zhang L,Lu C. 2011. YunFeechan BW, A, M,Yin Saidi NB,Le Bihan T, Yu M,Moore JW,Kang JG, KwonSpoel E, et SH,al. Yuan WC, HM,Liu Lu YT. 2017. SteudleYe Q, E. 2006. Wudick MM, ValentiniLi X, V, Geldner N, Chory J,Lin J,Maurel C,Luu DT. 2015. Wu J,Shang Wu Z, J,Jiang Moschou X, PN,Sun Roubelakis W, Wong HL, PinontoanHayashi R, K,Tabata R,Yaeno T, Hasegawa K,Kojima C, Yoshioka H, Iba K, Winterbourn CC. 2015. Winterbourn CC. 2014. – - J, Li X J,Li 25°C. 25°C. Rateconstants (M cana biosensor be for antioxidants. auxotrophy caused by the lack sup of 1445 signaling and H CALCIUM 200 737 catalase inrice:potential a switch to modulate intracellular H PlantCell production reactiveof oxygen species inABA Phospholipasedalpha1 and phosphatidic acid regulate NADPH oxidaseactivity and Biophysica Acta transgenictobacco plants with decreased iron superoxidedismutase. 264 2011. accumulation and JA biosynthesis in plantdefenses. Environment 1114. redistribution rootof aquaporins indu activated Ca Spermidine oxidase terminal extension. Kawasakiet T, al and Medicine reactive oxygen speciesin living cells. Oren , r - - - : : 41 In vivo D, Ratnasekera Wang D, C, Liu W 748. 268. -

- 1460. S Shamir M. 2013. - - nitrosylation NADPHof oxidaseregulates cell d 47.

- 21 DEPENDENT PROTEIN KINASE8 and CATALASE3function in reaction rates will courseof depend reactant on concentrations and pH. The

, Koziol, S,Krzepilko A,Bartosz G, Bilinski T. 2005. 2+ : : 2357

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: 459 The challengesThe of using fluorescentprobes to detectand quantify specific Are radicals free involved in thiol O - : 164

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CATALASE2 coordinatessa Do vacuolar peroxidasesact plant as caretakers?

Regulation of rice NADPH oxidaseby binding of Rac GTPaseto its N ortho

ht. All rightsht. All reserved. 19 2 - dihydroxy, 10 O

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X. X. 2016. regulatespol Journal of Biotechnology : 391 : eroxide dismutasein - ced by hydrogen peroxide. Biochimica biophysica et act X,Song L -- 4034. 2 - .

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- : : : - - O NO Heme peroxidases/catalase Peroxiredoxins/GPX/OxyR Fe enzymes Phenoliccompounds Methionine (Cysteine/GSH/Thioredoxin) Thiols Ascorbate This article isprotected bycopyrig summary NADPHof oxidase NADPH oxidaseactivity inresponse to environmental and developmental cues. See Fig. 3 for a These mechanisms providerapid a means activatingof inhibiting or superoxide/ H Table 2 producing hydroxyl radical. *Type III peroxidases catalase oxidation of phenolic compounds by 1). molecules. Nitric superoxide with thiols regenerated monodehydroascorbateradical and H contender for effectively removing superoxide the active.most Because ofrelatively its high concentration inplant cells, ascorbate coulda be 2 . - .

Accepted Article Abbreviations: GSH, glutathione, GPX,glutathione peroxidase; SOD, superoxidedismutase. Examples of modulation NADPHof oxidaseactivity by a variety interactingof factors.

oxide oxide (NO

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Calcium factors Interacting Calcium calmodulin 4 OST1/SnRK2.6 CIPK26 Calcium acid Phosphatidic DORN1 Nitric oxide XLG2 CPK5 BIK1 StCDPK5 OsRACK1 OsRac1

ht. All rightsht. All reserved. EF Activation through ? P phosphorylation Activation by EF Activation through Activation phosphorylation Activation by nitrosylation bindingS by Inhibition FAD of Activation phosphorylation Activation by phosphorylation Activation by EF Activation through on Effect activity phosphorylation Activation by Activation? EF Activation through

hosphorylation - - - - hand binding hand binding hand binding hand binding

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DHA and hydroxyl radical production and utilization in the NOX,NADPH oxidase; .

andfacilitated is by reduction Cuof R ). The ) ) ed arrows and outlineboxes

breakdown generatesH depends on the apoplast alkalinisation thatfollows ,

scavenging and transport.

( PRX Schwarzländer ot shown) ot and also directly released by some tion specificity.tion Attachment of CuZnSOD 2 - , ; s ; , nitrosoperoxycarbonate.

reaction H 2 O olid lines, reac 2 O 2

, initiate long distancesignalling. Akey 2 2

corbate and most thiols, except when O Superoxide 1 yellow removing enzymes O 2

) and) theirinteraction and, possibly,germin 2 , singlet oxygen; activated PRX The

ll. et al GPX, boxes,H , typeIII peroxidase; H

normal 2 O ., 2008 2 tions;

O ( glutathioneperoxidase 2 O 2 transport from in response to . Interaction of Cu , 2

. targets. CO - ) 2

PRX

Thediagram shows O dashed glutathioneredox and H ) . 2

; red; boxes,H Asc 2+ transportersnot

OH can

2

or Fe or . -

, PRX 2 and OH .

, hydroxyl O - as

likeproteins. produce O lines, with nitric 2 corbate;

3 are 3+

. to -

, Prx by .

and 2 + , . O

2 or or O 2 - 2 is 2 .

-

This article isprotected bycopyrig Accepted peroxidase. shown Prx; 1 oxidisewide a rang peroxidasesHaem form a parallel H with H targets and the chemical environment of cysteines within proteins which modulatestheir rea in sensing and signalling can achievedsubcellular by location sensors,of propensity to interactwith glutaredoxin/glutathione) could reduce ta transcription factor, target proteins could be oxidised directly. Thioredoxin (or andthiol disulfidestate. This paradigm is conserved across eukaryotesbut, in as thebacterial OxyR example MAP kinases) other enzymesor whose activity or subcellular releasetarget a protein, which could be a transcription factor protein kinase/phosphatase(for sulfenicac sensors (bluearrows) Fig. Article peroxidasethiol peroxiredoxin; RLK,receptor kinase; GLP, germin eATP, extracellular ATP; peroxidase; CDPK, Ca linesshow activation, inhibition or i other variously activate NOXand enzymeshave also been measured inapoplastic fluid. Hormones (e.g. facilitated by location inlipidGlutathione, rafts. ascorbate peroxidase localisation NOXof and its interactors, including signalling receptors and aquaporins, may be phospholi pHa could be factor.NOX activity depends on activation by Ca cytosol. Howthe O regulatory properties. know if localisation. Nota

4 - Dual roleDual of thiol peroxidases (TPXs)as hydrogen peroxide Cys Prx; PrxII, PrxQ and glutathioneperoxidase 2

in this example); O MnSOD, Mn superoxidedismutase; NOX,NADPH oxidase (RBOH); PRX 2 . Cysteineand pase D), phosphorylation and Rop id form ofTPX a interacts a with targetprotein

-

or NOXor isoenzymes expressed in different cells have significantly differentcatalytic or like protein; GPX .

ll the depicted reactions to occur the sameextent indifferentcells butwe do not 2 e . -

of substratesof in and H 2+ .

P - TPXs includeperoxiredoxins and glutathioneperoxidase dependent protein kinase; DAMP, damage olyamine oxidase TRX FAD, flavin adeninedinucleotide; glutathione ( 2 PRX O , t - like kinase; Rop, Rho 2 L hioredoxin

, glutathioneperoxidase forming activity is activated upon stimulation is unknown, although

butthese interactions are notshown in thediagram. Red pecked 2 O the ht. All rightsht. All reserved. GSH 2

removal system and, in the case of apoplast ;

nteractions. ( ) rgetprotein disulfidesto terminate signalling. Specificity CAT PAO

are - GTPasebinding ,

) relatively c

activity depends polyamineon transport from the atalase - and GTPase plants of in GDP or GTP -

like. vacuoles. TPX AO, ascorbate oxidase; APX,ascorbate - ; like;

APX poorly reactive with H via GEF, guaninenucleotide exchange factor; The r

MAPK, mitogen (see Table (see 2 for references)

, a disulfidebond which thenresolves to

a scorbate peroxidase 2+ eaction mechanism of 2 , phosphatidic acid (produced by ( H - associated molecular pattern; 2 O ,

t 2

hiol peroxidases(e.g. 2 ) abscisicacid ( location changesbetween the and ascorbate recycling

scavengers (redarrows)and P PRX i , phosphate; - activ , utiliseH 2 - O like enzymes. The ated protein 2 -

bound (see (see Table 1). ; ABA PRX - 2 ) . Spatial , Cys Prx is O ,

Prx

t form CK ype IIIype 2

to to , ) - ctivity Cys ; TPX,; This article isprotected bycopyrig Accepted Article ht. All rightsht. All reserved.

This article isprotected bycopyrig Accepted Article ht. All rightsht. All reserved.

This article isprotected bycopyrig Accepted Article ht. All rightsht. All reserved.

This article isprotected bycopyrig Accepted Article ht. All rightsht. All reserved.