The message of nitric oxide in cadmium challenged plants

PlantScience181 (2011) 612–620

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PlantScience

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Themessageofnitricoxideincadmiumchallengedplants

´z´aMagdalenaArasimowicz-Jeloneka, ,JolantaFloryszak-Wieczorekb,EdwardA.Gwózd

ab

DepartmentofPlantEcophysiology,FacultyofBiology,AdamMickiewiczUniversity,Umultowska89,61-614Pozna´n,Poland

DepartmentofPlantPhysiology,PoznanUniversityofLifeSciences,Wo y´nska35,60-637Pozna´n,Poland

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abstract

Articlehistory:

Received28January2011

Receivedinrevisedform22March2011Accepted28March2011Available online 6 April 2011

Keywords:Nitricoxide

CadmiumtoxicityHeavymetalstress

Programmedcelldeath

Duringthelastdecadeithasbeenfoundthatcadmium(Cd),oneofthemosttoxicelementsoccurringinpollutedenvironments,interfereswithnitricoxide(NO),amultifunctionalsignalingmoleculeinlivingorganisms.TheformationofNOhasbeendemonstratedinvivoinvariousplanttissuesexposedtoCdstress,butunfortunately,thetimeandintensityofNOgeneration,relativelyfrequentlyshowscon ict-ingdata.Whatismore,thereisstilllimitedinformationregardingthefunctionalroleofendogenouslyproducedNOinplantschallengedwithheavymetals.The rstpharmacologicalapproachesrevealedthatexogenouslyappliedNOcanalleviatecadmiumtoxicityinplants,promotingthedirectscavengingofreactiveoxygenspecies(ROS)oractivatingantioxidantenzymes.However,recentreportshaveindi-catedthatNOevencontributestoCdtoxicitybypromotingCduptakeandparticipatesinmetal-inducedreductionofrootgrowth.Inviewofthisheterogeneousknowledge,muchmorepuzzlingifweconsiderresults rstobtainedusingexogenousNOsources,thisreviewisfocusedmainlyontheimplicationofendogenousNOinplantresponsetoCdexposure.Furthermore,abasicdraftforNOmodeofactionduringcadmiumstressisproposed.

© 2011 Elsevier Ireland Ltd. All rights reserved.

1.Introduction

Cadmium(Cd)asanimportantenvironmentalpollutantisanon-redoxheavymetaltoxictohumans,animals,andplants[1–3].Becauseofitshighsolubilityinwateritisrapidlytakenupbyplantroots,inwhichthemostevidentphytotoxicsymptomsareobserved.Cadmiumtoxicitytoplantsisoftenassociatedwithdisruptionofvariousmetabolicprocesses,includinguptakeandtransportofwaterandnutrients,photosynthesisandrespiration.AlsoanatomicalandstructuralchangesinplanttissuesarelinkedtoCdphytotoxicity,e.g.cellwallimpregnationbyphenoliccom-pounds,degenerationofphloemsievetubes,thickeningofcellwallsupporttissues,reducedcambialactivity,stomatalclosureanddys-functionofthephotosyntheticapparatusinchloroplasts[4].Atthe

Abbreviations:APX,ascorbateperoxidase;CaM,calmodulin;CAT,catalase;Cd,cadmium;ET,ethylene;GSH,reducedglutathione;GSNO,nitrosoglutathione;H2O2,hydrogenperoxide;IAA,auxin;IRT1,ferrousirontransporter;JA,jas-monicacid;l-NAME,Nω-nitro-l-Arg-methylester;l-NMMA,N -Methyl-l-arginineacetatesalt;MTs,metallothioneins;NO,nitricoxide;Ni-NOR,nitrite:NOreductase;NOS-like,nitricoxidesynthase-like;NOX,NADPHoxidase;NR,nitratereduc-tase;ONOO ,peroxynitriteanion;O2 ,superoxideanion;PA,polyamines;PBITU,S,S -(1,3-phenylenebis(1,3-ethanediyl))bis-isothiourea;PCs,phytochelatins;PCD,programmedcelldeath;PRs,pathogenesis-relatedproteins;ROS,reactiveoxygenspecies;RNS,reactivenitrogenspecies;SA,salicylicacid. Correspondingauthor.Fax:+48618295808.

E-mailaddress:marasimowicz@wp.pl(M.Arasimowicz-Jelonek).

cellularlevelCdtoxicityismanifestedaschromosomalaberrationsaswellascellcycleanddivisionalterations[5–7].Cadmiumhasasimilarelectroncon gurationandvalencestatetozinc[8].Itmayreplacethismetalinstructuresreferredtoaszinc ngersandinthiswaydisturbthetranscriptionmechanism[9].AtthemetaboliclevelCd-inducedsignaltransductiontriggersROSproduction,whichconsequentlyindirectlypromotesoxidativestressbydiminishedantioxidantcellcapacity,leadingtooxidativedamage,whichcouldbeatleastpartiallyresponsibleforCdtoxicity[10].Plantmolecu-larresponsetoCdstressismanifestedbytheactivationofvariousstrategiestocopewithitstoxicity.Apartfromnon-speci cmech-anismsbeinginvolvedintheexpressionofstress-relatedproteins,phytoalexinsandsignalingmolecules,themainattentionofcurrentstudiesisfocusedonspeci cresponsesrelatedtotheactivationofdifferentmetaltransportersandmetal-thiolatecomplexformation(glutathioneGSH,phytochelatinsPCs)contributingtoCdtolerance.

Nitricoxide(NO)asamultifunctionalsignalingmoleculehasbeenthoroughlystudiedinplantsforover10yearsnow[11,12].AccordingtothepresentknowledgeplantspossesawiderangeofbiosyntheticNOpathways,whichcanbegenerallyclassi edaseitheroxidativeinoperation,suchasnitricoxidesynthase-like(NOS-like)activity,orreductiveinoperation,including,e.g.thenitratereductase(NR)pathway[13].Asithasbeendocumented,NOcontrolsabroadspectrumofplantgrowthanddevelopmentalprocesses,startingfromgerminationandendingwithsenescence.Furthermore,nitricoxideisinvolvedintheregulationofplantresponsestobothabioticandbioticstressconditions[14–16].

0168-9452/$–seefrontmatter© 2011 Elsevier Ireland Ltd. All rights reserved.doi:10.1016/j.plantsci.2011.03.019

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