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Nitric Oxide-Ethylene Crosstalk during Plant Growth and Abiotic Stress Responses PDF

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antioxidants Review Gasotransmitters in Action: Nitric Oxide-Ethylene Crosstalk during Plant Growth and Abiotic Stress Responses ZsuzsannaKolbert1,* ,GáborFeigl1 ,LucianoFreschi2 andPéterPoór1 1 DepartmentofPlantBiology,UniversityofSzeged,6726Szeged,Hungary;[email protected](G.F.); [email protected](P.P.) 2 LaboratoryofPlantPhysiologyandBiochemistry,DepartmentofBotany,UniversityofSaoPaulo, SaoPaulo05422-970,Brazil;[email protected] * Correspondence: [email protected] (cid:1)(cid:2)(cid:3)(cid:1)(cid:4)(cid:5)(cid:6)(cid:7)(cid:8)(cid:1) (cid:1)(cid:2)(cid:3)(cid:4)(cid:5)(cid:6)(cid:7) Received: 15May2019;Accepted: 5June2019;Published: 8June2019 Abstract: Since their first description as atmospheric gases, it turned out that both nitric oxide (NO)andethylene(ET)aremultifunctionalplantsignals. ETandpolyamines(PAs)usethesame precursorfortheirsynthesis,andNOcanbeproducedfromPAoxidation. Therefore,anindirect metaboliclinkbetweenNOandETsynthesiscanbeconsidered. NOsignalisperceivedprimarily through S-nitrosation without the involvement of a specific receptor, while ET signal is sensed by a well-characterized receptor complex. Both NO and ET are synthetized by plants at various developmental stages (e.g., seeds, fruits) and as a response to numerous environmental factors (e.g.,heat,heavymetals)andtheymutuallyregulateeachother’slevels. Mostofthegrowthand developmentalprocesses(e.g.,fruitripening,de-etiolation)areregulatedbyNO–ETantagonism,while inabioticstressresponses,bothantagonistic(e.g.,dark-inducedstomatalopening,cadmium-induced celldeath)andsynergistic(e.g.,UV-B-inducedstomatalclosure,irondeficiency-inducedexpression ofironacquisitiongenes)NO–ETinterplayshavebeenrevealed. Despitethenumerouspiecesof experimentalevidencerevealingNO–ETrelationshipsinplants, thepictureisfarfromcomplete. UnderstandingthemechanismsofNO–ETinteractionsmaycontributetotheincrementofyieldand intensificationofstresstoleranceofcropplantsinchangingenvironments. Keywords: abioticstress;ethylene;growthanddevelopment;nitricoxide 1. Introduction 1.1. Biochemistry,Synthesis,Storage,andTransportofNOandETinHigherPlants Nitric oxide (NO, N=O) is one of the smallest diatomic gas (30.006 g mol−1), containing a doublebondbetweentheNandtheOatoms,withactiveredoxcharacterduetothepresenceofone unpairedelectron[1]. Ethylene(ET,C H ,CH =CH )isalsoasmallandsimplegaseousmolecule 2 4 2 2 (28.054gmol−1),containingtwoCatomswithadoublebondandnoradicalcharacterorredoxnature. BothNOandETaresmall,unchargedandlipophilicmolecules;therefore,theyarecapableofdiffusing acrossmembranesandtraveleasilyfromcelltocell. EarlyreportsdescribedNOasanatmosphericgasinfluencinggrowthofaerialplantparts[2–5]. InthecaseofET,thesameconclusionwasdrawnintheearlystudies;however,theseobservations weremademuchearliercomparedtoNO(in1858and1901,[6]). Untilthe1960s,ETwasexclusively examinedasapromoteroffruitripening;however,intenseresearchonETinfluenceonothergrowth responseswassubsequentlystarted[7–10]. Therefore,ETresearchprecededNOresearchsincethe secondphaseofNO-relatedplantstudiesonlybeganinthe1990s. Antioxidants2019,8,167;doi:10.3390/antiox8060167 www.mdpi.com/journal/antioxidants Antioxidants2019,8,167 2of22 Inhigherplants,theproductionofNOistightlyconnectedtoplantnitrateassimilation[11]where reductivereactionsleadtoNOformation. Nitratereductase(NR)wasshowntodirectlyreducenitrite to NO; however, its NO-producing activity is only 1% of its nitrate-reducing activity invitro [12]. AnindirectroleNRinNOproductionhasalsorecentlyemerged,basedontheNR-mediatedtransfer ofelectronsfromNAD(P)HtotheNO-formingnitritereductase(NOFNiR)whichinturncatalyzesthe invitroandinvivoreductionofnitritetoNO[13]. However,thesignificanceofNR-NOFNiRsystemin NOsynthesisduringstressresponsesstillremainstobeelucidated. BesidesNR,root-specificnitrite:NO reductase(NiNOR)[14]wereshowntoproduceNOusingnitriteasasubstrate. Non-enzymaticNO synthesishasalsobeendemonstratedunderspecificconditions,suchasintheapoplastofbarleyseed aleuronelayerwherenitriteisreducedatacidicpHinthepresenceofascorbateleadingtotheformation ofNO[15]. Oxidationofreducednitrogencompounds(L-arginine,polyaminesorhydroxylamine)is anadditionalwaytoreleaseNObyplanttissues. Usingbiochemicalapproaches,L-arginine-dependent NOformationwasdetectedindifferentplantspecies[16];althoughthegeneformammalian-likenitric oxidesynthase(NOS)enzymehasnotbeenidentifiedinlandplantseversince[17]. Therefore,Corpas andBarroso[18]arguethehypothesisthatL-arginine-dependentNOS-likeactivityinhigherplants couldbetheresultofcooperationbetweendiscreteproteins. Incontrasttohigherplants,inalgaelike OstreococcustauriandSynechococcusPCC7335NOSenzymesfunctionallyandstructurallysimilarto mammalianNOShavebeencharacterized[19,20]. Also,polyamines(PAs)aregoodcandidatesfor oxidativeNOrelease;however,themechanismisstillunclear. Copper-amineoxidase1(CuAO1)was foundtobeinvolvedinPA-inducedNOformationascuao1-1andcuao1-2mutantsshowedprevented PA-inducedNOformation[21]. Later,Großetal.[22]foundthatlowNOlevelofcuao8Arabidopsis is associated with increased arginase activity, which can contribute to lower NO production due to poor availability of arginine. An important precursor of PA synthesis is S-adenosylmethionine (SAM) [23], which is also the substrate for ET biosynthesis. In the first step, SAM is converted to 1-aminocyclopropane-1-carboxylicacid(ACC)bytheenzymeACCsynthase(ACS).Theotherproduct ofACSactivityismethylthioadenosine,whichisrecycledtomethionine(Met)intheYangcycleto maintainintracellularMetlevel. TheACCisthenoxidizedbyACCoxidase(ACO)inthepresence ofFe(II)cofactor,oxygenandascorbateresultingintheevolutionofET,CO ,andHCN.Therefore, 2 comparedtootherplanthormones,thebiochemicalpathwayofETsynthesisinplantsseemstobe relativelysimple. BothACSandACCareencodedbymultigenefamiliesandthemRNAlevelsand activityofeachisoenzymearedifferentlyregulatedbyendogenous(e.g.,auxin,NO)andenvironmental factors (e.g., flooding, drought, pathogen attack) [24]. The relationship between the biosynthetic pathwaysofNOandETisdepictedinFigure1. Asdiscussedabove,itiswidelyacceptedthatNOcanbesynthesizedinhigherplantsbyoxidative andreductivemechanismsinvolvingenzymesandalsonon-enzymaticprocesses. Thesubstratesfor oxidativepathwaysincludeaminoacids(L-arginine)orcompoundscontainingtwoormoreaminoacids (polyamines). The copper amine oxidase-catalysed degradation of PAs leads to NO production. DuetothecommonprecursorofPAandETsynthesis(SAM),theNOandETsynthesisarelinkedvia PAmetabolism. BothNObiosynthesisandremovalarecriticallyimportanttoregulatesteady-stateNOlevels in plant cells. In the presence of molecular oxygen, NO forms nitrite and nitrate, and it interacts − with superoxide anion to form peroxynitrite (ONOO ) [25]. Moreover, NO may also react with proteins,likehemoglobin(Hb),andthisinteractionfacilitatesitsoxidationtonitrate[26,27]. Another possiblemechanismforNOremovalinvolvesNRenzymewhichcantransferelectronstothetruncated hemoglobinTHB1catalyzingtheconversionofNOintonitratebyitsdioxygenaseactivity[11,28]. NO can initiate S-nitrosation reactions with thiol (SH)-containing proteins and peptides resulting in the formation of low-molecular-weight S-nitrosothiols such as S-nitrosocysteine (CysNO) or S-nitrosoglutathione(GSNO)[29,30]. TheS-nitrosothiolsliberateNOandparticipateintransnitrosation or S-thiolation [29,31]. The most abundant S-nitrosothiol is GSNO which can non-enzymatically generateNOorbereducedbytheenzymeS-nitrosoglutathionereductase(GSNOR),yieldingoxidized Antioxidants2019,8,167 3of22 glutathione(GSSG)andammonia(NH )[32]. BesidesbeinganintracellularNOreservoir,GSNOmay 3 alsobetransportedbetweencells,tissues,andorgansimplementinglong-distancetransportofNO signal[33]. In the case of ET, the inactivation by oxidation is not physiologically relevant in regulating steady-stateETlevelsduetoitsfastdiffusionfromtissues. ShortdistancemovementofEToccurs viadiffusionfromcellsintointercellulargasspacesandintotheenvironment,whileitslong-distance Atnrtaionxsidpaonrtst 2f0r1o9m, 8,i xs FpOrRo vPeEdERt oREbVeIEAWC C[34]. 3 of 23 FFigiguurree 1.1 S.cheSmchateimc oavtiecrvoievwer voife wethyolfeneet hsyylnetnheesissy innttheersmisediinatteersm (Se-daidaetensos(ySl--amdeetnhoiosnyiln-me,e SthAiMon;i n1-e, aSmAiMno;c1y-calompirnoopcayncelo-1p-rcoaprbaonxey-1li-cc aarbciodx, ylAicCaCc)i da,nAdC Cen)zaynmdees n(zAymCCes s(yAnCthCassey,n tAhCasCe ,oAxCidCasoex).i dTahsee) . fTorhmeafotiromn aotfi onnitroifc noixtirdice othxridouegthhr pouutgrhespciunter e(sPcUinTe) (oPxUidTa)tiooxni dbayt cioonppbeyr-caomppineer--oaxmidinaes-eo (xCiduaAsOe)( Cisu aAlsOo ) diespaiclsteod;d heopwicetevde;r, hthoew qeuveesr,tiothne mqaurkes itniodnicamteasr kthaint dthicias tmesecthhaantisthmis remquecirheasn fiusmrtherer qeuxipreesrimfuerntthaelr eevxipdeernicme.e nAtadldeivtiiodneanlc ea.bAbrdedviitaiotinoanlsa: bLb-rMeveita,t iLo-nms:eLth-Mioneti,nLe;- mSeAtMhioDnCin, eS;ASAMM dDeCca,rSbAoMxydlaescea; rbdocxSyAlMas,e ; ddeccSaArbMox,ydleacteadrb SoAxyMla, tSePdDS,A spMe,rmSPidDi,nsep; eSrpmdiSd, isnpee;rSmpiddSin,sep seyrnmthidasine;e SsPyMnt,h sapseer;mSPinMe;, SsppmerSm, isnpee;rSmpimneS , ssypnetrhmasien.e synthase. 1.2. PerceptionandTransductionofNOandETSignals As discussed above, it is widely accepted that NO can be synthesized in higher plants by oxidaDtivuee taontdh ereladcukcotifvken omwenchsapneicsimficsr eincevpotlovrisn,gp eernczeypmtioens aannddt raalnsosd nuocnti-oennozfyNmOatisci gpnraolcaersesbees.l ieTvheed stuobrsetlryatoens fpoors ottxriadnastliavteio pnaatlhmwoaydsifi incactliuodnes a(PmTinMosa)csidusc h(La-sarSg-ninitirnoes)a otiro cno,mtyproousinndesn ciotrnattaioinninagn dtwmoe otar l mniotrreo saymlaitnioonacoifdtsa (rpgoetlyparmotieniness)[.3 T5h].eS c-onpitproesr aatmioinnies oaxriedvaesres-icbaletacloyvseadle ndtergeraacdtiaotnioanff oefc tPinAgs clyeastdesi ntoe tNhiOo l pgrrooduupcstiaonnd. cDounes etqou tehnet lcyommomdoifny ipnrgecpurrostoeirn oaf cPtiAvi tayn,dlo EcaTl iszyantitohneosirs i(nStAerMac)t,i othnes. NTOhi saPnTdM ETis scyantathlyezseisd + abrye lhinigkheedr voixaid PeAs omfeNtaOboolrisnmitr. osoniumcation(NO ),metal-NOcomplexes,andlowmolecularweight S-nitBroostho tNhiOol sbi(oCsyysnNthOe)siosr aGnSdN reOm[o3v6]a.l Aarcec ocrridtiincaglltyo itmhepomrotasnttc otom rpegreuhlaentes isvteeaddayt-assteatteo fNSO-n lietrvoeslas tiend pplarontte cinelsl,s.1 ,I1n9 t5heen pdroegseenncoeu oslfy mSo-nleictruolsaart oedxypgeepnt,i dNeOs bfoerlomnsg ninitgrittoe a9n26d pnritortaetien, sacnadn itb einftoeurancdts iwnitthhe sAurpaebriodxopidsies apnroioteno tmo efo[r3m7] .peroxynitrite (ONOO−) [25]. Moreover, NO may also react with proteins, − like hMemooregolovbeirn, N(HOb)c,a anndin tflhuise nincteerparcottieoinn faacctiilvitiattyesin idtsi roexcitdlyattihorno tuog nhittrhaetef o[2r6m,2a7t]i.o AnnooftOheNr OpoOssiibnlea mreeacchtaionniswmi thfosru NpeOro rxeidmeo.vPaelr oinxyvnoiltvreitse NfoRrm eantzioynmlee awdshtiochp rcoatne intratynrsofseirn eelneicttrraotniosn t(oP TthNe) .tPruTnNcaisteadn hierrmevoegrlsoibbilne tTwHo-Bs1te cpaPtaTlMyzidnugr itnhge wcohnicvhearsnioitnro ogf rNouOp i(n-NtoO n2i)tbrainted sbtyo itthse dairooxmygateincarsineg aocftitvyirtoys i[n1e1,(2T8y]r. ) NinOt hcaeno ritnhiotipatoes iSt-inonitrroessautlitoinng reinactthioenfso rwmitahti othnioolf (3S-Hni)t-rcootnytraoisniinneg[ p38ro].teIninps laanndt cpeellpst,iPdTesN reinshuilbtiintsg tihne tahcet ivfoitrymoaftitohne poafr tliocwul-amroenlezcyumlaer-pwroeitgeihnt aSs-rneivtrioeswoethdioinls[ 3s9u].chT yaros sSin-neintriotrsaotcioynstmeinaye e(iCthyesrNpOre) voern tSo-r niintdrouscoegtlhuetatythroiosninee p(hGoSspNhOo)r yla[2ti9o,n30;t]h. usT,hitec anSi-nnflituroensoctehcieolllss iglnibaellriantge [39N].OIn aacnodm ppreahrteincsipivaetes tuidny , transnitrosation or S-thiolation [29,31]. The most abundant S-nitrosothiol is GSNO which can non- enzymatically generate NO or be reduced by the enzyme S-nitrosoglutathione reductase (GSNOR), yielding oxidized glutathione (GSSG) and ammonia (NH3) [32]. Besides being an intracellular NO reservoir, GSNO may also be transported between cells, tissues, and organs implementing long- distance transport of NO signal [33]. In the case of ET, the inactivation by oxidation is not physiologically relevant in regulating steady-state ET levels due to its fast diffusion from tissues. Short distance movement of ET occurs via diffusion from cells into intercellular gas spaces and into the environment, while its long-distance transport from is proved to be ACC [34]. Antioxidants2019,8,167 4of22 127nitratedproteinswereidentifiedinwild-type,controlArabidopsisthaliana[40]indicatingthatplants possessaphysiologicalnitroproteome[39]. Nitricoxidecanalsobindtotransitionmetalionslikeiron (Fe2+orFe3+),copper(Cu2+)orzinc(Zn2+)inmetalloproteinstoformmetal-nitrosylcomplexes[41]. Thebiologicalsignificanceofmetalnitrosylation;however,needstobefurtheranalysed. ContrarytoNOsignalling,ETperceptionandsignallinginvolvethefunctionofspecificreceptors. ETisperceivedbyareceptorcomplexlocatedintheendoplasicreticulummembrane,whichisrelated tothehistidineproteinkinasereceptorsofthetwo-componentsignallingsystemfoundinprokaryotes. InArabidopsis,fiveETreceptorshavebeenidentified(ETHYLENERECEPTOR1and2,ETR1,ETR2; ETHYLENE RESPONSE SENSOR1 and 2, ERS1, ERS2; ETHYLENE INSENSITIVE4, EIN4). The N-terminaltransmembranedomainofthereceptorsbindsETinthepresenceofacopperco-factor. WithoutET,thereceptorsactivateaserine/threonineproteinkinaseCONSTITUTIVERESPONSE1 (CTR1), which in turn negatively regulates the downstream ethylene response pathway, possibly throughaMAP-kinasecascade. OnceETbindingtakesplace,thereceptorsbecomeinactive,resultingin deactivationofCTR1,whichinturncausesETHYLENEINSENSITIVE2(EIN2)tofunctionasapositive regulatorofETsignalling. EIN2containstheN-terminalhydrophobicdomainandthehydrophilic C-end, and positively regulates nucleus-located ETHYLENE INSENSITIVE3 (EIN3) transcription factors(TFs). EIN3bindstothepromoterelementofETHYLENERESPONSEFACTOR(ERF1)gene and activates its transcription in an ET-dependent manner. Transcription factors like ERF1 and other ethylene-response-element binding proteins (EREBPs) can interact with the GCC box in the promoteroftargetgenesandactivatedownstreamETresponses[24]. Evidenceindicatesthatgroup VII of the ERF/AP2 transcription factor family (i.e., ERFVIIs) may be implicated as sensors of NO availability during early seedling development (i.e., seed germination and hypocotyl elongation) and stomatal closure [42]. It has been shown that ERFVII-dependent NO sensing relies on the specificoxidationoftheC2residueoftheseTFs,leadingtotheirarginylationandpolyubiquitylation and subsequent proteasomal degradation via the N-end rule proteolytic pathway. Whether the NO-dependent modulation of ERFVII stability is a central mechanism controlling other NO–ET interactionsthroughouttheplantlifecycleremainstobeinvestigated. Basedontheabove,NOandETsignaltransductionmechanismsinplantcellsarefundamentally different. NOhasnospecificreceptor; thustheNOsignalisperceivedattheproteomelevel, and itleadstosignaltransductionandgeneexpressionresponseprimarilyviaspecificPTMs. Contrary toNO,ETsignalissensedbyawell-characterized,specificreceptorcomplex,havingthenegative regulationinitssignallingcascadeasdistinctivecharacteristic. ETisconsideredtobeaclassicalplanthormonebecauseitisdetectedthroughspecificreceptors andactsatlowconcentrations(0.01to1.0ppm)[43]. Ontheotherhand,sincetheNOsignalisnot perceivedbyspecificreceptorsandtherangeofitseffectiveconcentrationisapparentlyhigherthan those of the classical phytohormones, we presently do not consider NO as a plant hormone, but insteaditisregardedasanon-traditionalgrowthregulatorthatactsininteractionwithtraditional phytohormones,includingET,duringplantgrowthanddevelopment. Thefurthersectionsofthis review intend to discuss these wide-scale interactions between NO and ET in plant growth and developmentundereitheroptimalorstressfulconditions. 2. NO–ETInterplayduringPlantDevelopment Inconjunctionwithotherregulatorysignals,NOandETareknowntoinfluenceavastarrayof developmentalprocessesduringtheplantlifecycle. Overtheyears,thesetwogaseoussignalshave beendemonstratedtocloselyinteracttocontrolkeybiologicalprocessesinearlyplantdevelopmentas wellasinvegetativegrowth,fruitripeningandleafsenescence(Figure2). Antioxidants2019,8,167 5of22 Antioxidants 2019, 8, x FOR PEER REVIEW 9 of 23 FFigiguurree 22.. NNiittrriicc ooxxiiddee ((NNOO))--eetthhyylleennee ((EETT)) iinntteerraaccttiioonnss dduurriinngg ppllaanntt ggrroowwtthh aanndd ddeevveellooppmmeenntt.. SSyynneerrggisistitcici ninteterrpplalayyw waassi ninddicicaateteddi ning grreeeenn,,w whhilielea anntataggoonnisismmw waassi ninddicicaateteddi ninr reedd..A Abbbbrreevviiaattiioonnss:: AACCSS,,1 1-a-ammininooccyycclolopprrooppaannee-1-1-c-caarrbbooxxyylliicca accidids syynnththaassee,,A ACCOO,,a ammininoocycycclolopproroppaannee-1-1-c-caarrbbooxxyylilcica accidid ooxxididaasese;;S ASHAaHsea,saed, enadoseynlohsoyml ohcoymstoeicnyasstee;inMaEseT; syMnEthTe tassyen,tmheetthasioen, inmeestyhniothneintaes e;sMynAthTe,tmaseeth; ioMniAnTe, adenosyltransferase;LR,lateralroot;AR,adventitiousroot. methionine adenosyltransferase; LR, lateral root; AR, adventitious root. 2.1. NO–ETCrosstalkduringSeedGermination 3. NO–ET Interplay in Abiotic Stress Responses Theultimategoalofzygoticembryogenesisistoproduceaviableseed,whichhasthecapacity Environmental stresses (e.g., excess light, cold, heat, salt, drought, flooding, nutrient togerminate. Environmentalfactors,includingtemperature,wateravailabilityanddaylength,play deficiencies, heavy metals) are relevant determinants of plant physiological processes. Plant a crucial role in the maintenance and break of seed dormancy, whose main function is to prevent responses to these abiotic stresses are regulated by crosstalk between multiple signal molecules, germination when circumstances are not favouring seedling survival [44]. Beyond the effects of including NO and ET (Figure 3). environmentalfactors,seeddormancyisalsocontrolledbynumerousendogenousfactors;primarily associatedwithchangesinthebalanceofthehormonesabscisicacid(ABA)andgibberellins(GAs)[45]. Due to its crosstalk with ABA and GA, ET is also involved in seed development [46], having a well-knownroleintheremovalofseeddormancyandpromotionofgermination[47,48]. Similarly, NOalsoinducesgerminationinnumerousplantspecies[15,49,50]andthealeuronelayerseemstobe relevantinNOgenerationandsignalling[51]. Ingeneral,asynergisticlinkseemstoexistbetweenNOandETduringseedgerminationatvarious levels [52]. Besides counteracting ABA-imposed seed dormancy [53] and facilitating the onset of GA-stimulatedgermination[51],NOhasalsobeenshowntopromotethebreakingofappleembryonic dormancy by stimulating ET emission [54]. The NO-triggered release of apple embryo dormancy correlatedwithenhancedETproductionandwasabolishedwhenETsynthesiswasinhibited[54]. Inlinewiththis,subsequentstudiesdemonstratedthattheNO-triggeredincrementinETproduction ingerminatingappleembryoswasassociatedwiththestimulationofbothACSandACOactivities[55]. Altogether,thesefindingsindicatetheinvolvementofendogenousETproductioninNO-triggered dormancybreaking. Antioxidants2019,8,167 6of22 In the case of Amaranthus retroflexus seeds, the germination was induced by exogenous NO, andthiseffectwasprecededbyincreasedETproduction,indicatingthattheNO-induceddormancy breakingisalsoET-dependent. Ontheotherhand,ET-inducedseedgerminationhasalsobeenshown torequireNOpresence. Moreover,bothNOandET-inducedseedgerminationwereassociatedwith theactivationofthecellcyclebeforeradicleemergence[56]. 2.2. NO–ETInterplayduringVegetativeGrowth Asamultifunctionalplanthormone,ETcaneitherstimulateorinhibitplantgrowthdepending onitsconcentration,onthedurationoftheapplicationandtheplantspecies[57]. Accordingtomany reports,theinteractionbetweenNOandETtendstobemoreantagonisticduringplantvegetative growth;however,itlargelydependsontheexactprocessororganinvestigated[58]. Duringlight-inducedgreeningandchloroplastdifferentiation,eitherendogenouslyproducedor exogenouslyappliedNOwasfoundtopromotethesede-etiolation-relatedprocessesbyinhibiting ACOactivityandconsequentlyrepressingETbiosynthesis(andinducingauxinsynthesis)intomato (Solanumlycopersicum)cotyledons. Furthermore,pharmacologicalandgeneticapproachesrevealed that higher ET levels inhibited NO formation and total NR activity, suggesting a mutual negative interactionbetweenETandNOsignallingduringde-etiolationoftomatoseedlings[59]. TranscriptomicandgeneticevidencebasedonArabidopsissensitivitytoNOinhypocotylshortening furtherindicatedthatNOandETsignallingareconnectedduringearlyseedlingdevelopment[60]. Remarkably,theethylene-insensitivemutantsetr1-3andein2-5mutantswerecompletelyinsensitiveto exogenousNO-inducedhypocotylshortening,therebyprovidingfurthersupporttotheinvolvement ofETsignallinginNOsensingduringearlyseedlingdevelopment. FewreportsdescribetheET-NOinteractioneventsduringrootdevelopment. Ethylenenegatively regulateslateralroot(LR)initiation,growthandelongationinArabidopsis[61,62],whileNOwasfound toinduceLRgrowthintomato[63]. Recently,itwasobservedthatNO-inducedLRinitiationpossibly reliesontheinhibitionofACOinsunflowerseedlings. AuthorshypothesizedseveralwaysofNO action: (1)NOmaymodifytheferroussiteofACOleadingtoitsinhibition,(2)NOmayinhibitthe expressionofACOgenes,and/or(3)NOmaymodifytheexpressionoftranscriptionfactorsleadingto reducedACOgeneexpression[64]. Moreover,inselenium(Se)-stressedrootsystemofArabidopsis,the incrementinLRemergencewasaccompaniedbyelevatedETlevelswhichwereshowntoinhibitNO production. ExogenousNO(GSNO)decreasedETlevelssuggestingamutuallynegativeinterplay betweenNOandETduringSe-inducedLRemergence[65]. BothNOandETalsoplayaroleintheinductionofadventitiousroot(AR)development[66–68]. AsarareexceptioninvestigatingNO–ETcrosstalk,Jinetal.[69]reportedthatexogenousapplication of ethylene-releasing compound 2-chloroethylene phosphonic acid (ethephon) induced both AR formation and NO production in marigold (Tagetes erecta) whereas scavenging of NO (by cPTIO) significantlyinhibitedAR-inducingcapacityofethephon. TheauthorsconcludedthattheAR-inducing effectofETreliesonendogenousNOgenerationinmarigoldroots[69]suggestingasynergismbetween ETandNOinthisprocess. Atthecellularlevel,ET-NOinteractionwasinvestigatedinArabidopsiscellculture[70]. BothNO andETwereproducedbywild-type(WT)cellcultureintheperiodofactivecelldivisionwhileein2 cellsfailedtoproduceETbutemittedincreasedNOlevels. Moreover,lowconcentrationsofNOdonor (SNP)stimulatedG1/SphasetransitionandreducedETlevelsinWTArabidopsiscells,suggestingan antagonisticrelationshipbetweenETandNOlevelsduringcellcycleprogression. HigherNOdonor concentrationsrestrainedSphasetransitionindicatingtheconcentration-dependenteffectofNOon celldivision. Interestingly,ein2cellswereinsensitivetoalowdosageofNOdonorsuggestingthatthe effectofNOoncelldivisioninvolvesEIN2-associatedETsignalling. Antioxidants2019,8,167 7of22 2.3. NO–ETInteractionduringReproductiveGrowth AlthoughbothNOandEThavebeenreportedtorepressfloraltransitioninArabidopsis[71,72] whetherthesesignallingmoleculescrosstalktointegrateexternalandinternalsignalsintothefloral decision remains to be investigated. NO is actively produced during floral development until anthesis [73], and Arabidopsis mutants with altered NO levels usually display limited fertility [74]. AchemotropicrolehasbeenattributedtoNOduringpollentubenavigationandovuletargeting[75], which may be one of the reasons behind the low fertility, reduced silique size and limited seed productioninArabidopsismutantswithdisturbedNOlevelssuchasthenitricoxideoverexpression1 (nox1)andtheAtGSNOR1loss-of-functionatgsnor1-3[72,74]. Amongfleshyfruits,reducedfruitsize associatedtoincreasedendogenousNOlevelshasalsobeenreportedforthetomatomutantshortroot (shr),whichalsodisplayedmarkedreductioninflowersizeandfertility[76]. Thoughevidenceindicates thatETinfluencesplantsexualreproductionviamultiplemechanisms,includingtheregulationof pollentubegrowth[77],ovulelifespan[78]andfruitset[79],somepotentialNO–ETcrosstalkduring theseresponsesremainselusive. SincetheseminalstudiescarriedoutbyLeshem’sgroup[80,81],NOhasemergedasapotent moleculecapableofextendingshelf-lifeofpostharvestfruitsofseveralimportantcropspecies([82]and referencestherein),actingasanantagonistofETinmanyofthesecases. Ripening-associatedprocesses typicallypromotedbyET,suchascellwallsoftening,chlorophylldegradationandsynthesisofnew pigments,areinhibitedordelayedbyNOtreatment[83],therebyleadingtoanextensioninpostharvest fruitshelflife([84]andreferencestherein). Biochemicalroutesleadingtothesynthesisofimportant fruit nutritional compounds, such as carotenoids, flavonoids, and ascorbate, also are under strict regulationbytheNOandETinterplay. Forexample,carotenoidsynthesisandascorbicaciddegradation arebothpromotedbyET[85,86]andinhibitedbyNO[87,88]duringfruitripening. Therefore,the finalnutritionalattributesoffruitswillultimatelydependonthecombinedinfluenceofthesetwo gasotransmittersduringtheripeningandpost-ripeningphases. Moreover,NOtreatmenthasalsobeen showntodelayoramelioratethedevelopmentofphysiologicaldisordersanddiseaseincidenceduring postharveststorage,particularlywhencombinedwithlow-temperatureconditions[84,89]. In contrast with the wealth of information about ET biosynthesis and signalling during fruit ripening,dataonNOmetabolisminripeningfruitsremainrelativelyscarce. Byemployingnon-invasive photoacousticspectrometry,LeshemandPinchasov[81]revealedanoppositetrendbetweenNOandET emissionratesduringbothclimactericandnon-climactericripening,withNOandETpredominating inthegreenandripestage,respectively. Inagreement,endogenousACCandNOlevelsdisplayedan inversecorrelationduringtheabscissionofmatureolive(Oleaeuropaea)fruits[90]. Inpepper(Capsicum annuum), the transition from green to red stage is associated with a decline in NO levels and the accumulationofbothnitrosatedandnitratedproteins, whichalsocoincidedwiththereductionin GSNORactivity[91,92]. Intriguingly, althoughfruitsofNO-hyperaccumulatortomatomutantshr displayedslowerripeningcomparedtoWTcounterparts,nosignificantdifferencesinETemission wereobservedbetweenshrandWTfruitsattheclimactericphase[76]. Climacteric fruits, which strongly relies on ET signalling for ripening initiation, predominate amongtherepresentativeexamplesofNO–ETantagonismduringripening,includingseveralmajor fleshyfruitcropssuchasapple[93],banana(Musaspp.,[94]),tomato[87],papaya(Caricapapaya,[95]), peach(Prunuspersica,[96])andmango(Mangiferaindica,[97]). Inthesefruits,theclimactericpeakof ETproductioniseitherreducedordelayedinresponsetoNOtreatment[87,94],aresponsefrequently associatedwithNO-triggeredreductionsintranscriptabundanceandactivityofkeyETbiosynthetic enzymes,particularlyACSandACO[97]. Insomecases,thelowerACOandACSactivitiesdetected inNO-treatedfruitswereatleastpartiallyexplainedbythedeclineintheirencodingtranscripts[87,94]. However,thedirectinhibitionofACSandACOviaNO-mediatedPTMcannotberuledout[58]. NO-mediatedPTMeventsareassumedtoaffectSAMturnoverinplantsasthemethylmethionine cycle enzymes adenosyl homocysteinase (SAHase), methionine synthase (MET synthase) and methionineadenosyltransferase(MAT)haveallbeenidentifiedascommontargetsofS-nitrosation Antioxidants2019,8,167 8of22 in GSNO-treated Arabidopsis leaf extracts [98]. Further support for MET synthase as a target of S-nitrosationwasprovidedwhenthebiotin-switchtechniquewasconductedinGSNO-treatedleaf extractsofotherspecies,suchasKalanchoëpinnataandBrassicajuncea[99,100]. Moreover,Lindermayr etal.[101]havedemonstratedthatArabidopsisMAT1activityisinhibitedbyS-nitrosationatCys-114 underinvitroconditions. ItisalsopossibletoconceivemorecomplexscenarioswhereNOinhibitsfruitETbiosynthesis viaintermediarysteps. NOisacentralplayerinplantredoxmetabolismandhomeostasis[102],and theactivityofantioxidantenzymessuchascatalase(CAT)andascorbateperoxidase(APX)canbe modulatedviaS-nitrosationduringfruitripening[103]. AsbothfruitripeningandETbiosynthesisare influencedbyredoxsignalling[83],anindirectactionofNOonripeningviachangesonfruitredox stateremainsanunexploredpossibility. Moreover,hydrogensulfide(H S)hasbeenrecentlyproposed 2 as part of the NO–ET crosstalk in ripening fruits, with NO and H S synergistically interacting to 2 inhibitETproductionduringfruitripening[82,103,104]. EvidenceindicatesthatH Scanacteither 2 upstreamordownstreamNOdependingonthephysiologicalprocessconsidered[103],andH Shas 2 beenproposedtoreduceETproductionintomatoplantsbyinhibitingACOactivityviapersulfidation ofCys-60[77]. Therefore,acomplexinterplaybetweenNO-H S-ETmaybeinvolvedinfruitripening, 2 andthisemerginginterplaycertainlydeservesfurtherinvestigation. 2.4. NO–ETInteractionduringSenescence ETislargelyacceptedasakeypromoterofleaf,flowerandfruitsenescence,whereasNOplays anoppositerole[58]. Thesenescence-promotingroleplayedbyETisconfirmedbythepremature senescencesymptomssuchasleafyellowing,necrosisandabscissiontriggeredinmanyspeciesupon ET exposure [57]. The rise in endogenous ET production during both natural and stress-induced senescenceaswellasthealteredsenescencephenotypeofmanyETbiosynthesisandsignallingmutants alsosupportthepromotiveeffectofETonleafsenescence[57]. Similarly,climactericETproductionis triggeredinmanyflowerssoonafterpollination,leadingtowilting,fadingandabscission,whereasthe treatmentofflowerswithinhibitorsofETbiosynthesisoractionfrequentlyleadstodelayedsenescence ([105]andreferencestherein). Incontrast,NOfumigationortheexposureoftheplantstoconditionsthatpromoteendogenous NOlevels(e.g.,highnitrate)usuallydelayleafsenescence[105],andtreatmentsofflowerswithNO donorshavelongbeendescribedtoextendtheirvaselife[106]. Moreover,leafsenescenceisaccelerated wheneverendogenousNOcontentisreduced,suchasinNO-deficientmutants[107]andtransgenic plantsoverexpressingaNO-degradingdioxygenase(NOD)gene[108]. Youngplanttissuesusually displayhigherNOlevels, whichprogressivelydecreaseasplantorgansmature[109,110], withET displayinganoppositetrend[111]. Therefore,plantETandNOmetabolismsseemtobeinversely influencedbytissueaging. LittleisknownaboutthemechanismsbehindtheNO–ETcrosstalkregulatingleafandflower senescence. Inlinewiththeapparentantagonisticrelationshipbetweenthesegasotransmittersduring senescence, the leaf senescence-like phenotype of NOD-expressing Arabidopsis transgenic plants coincided with increased expression of AtACS6 [108], which is one of ACS genes responsible for the enhanced ET production during leaf senescence in this species [112]. More recently, Niu and Guo[113]providedgeneticevidencebasedontheuseofboththeNO-deficientmutantAtnoa1and ethylene-insensitivemutantein2-1suggestingthattheNOactionduringdark-inducedsenescencein Arabidopsisinvolvesethyleneinsensitive2(EIN2), whichapositiveregulatorofETsignallingand leafsenescence[114]. TheprematuresenescenceobservedintheNO-deficientAtnoa1mutantwas attenuatedbymutationsinEIN2,andthedark-triggeredinductionofsenescencemarkergenesand thylakoidmembraneintegritylosswassignificantlydelayedintheAtnoa1ein2-1doublemutant[113]. Incutflowers,theincrementofvaselifeuponNOtreatmentalsoseemstoinvolveanantagonistic influenceofthisfreeradicalontheETbiosyntheticpathway. BesidescounteractingtheETpromotive effectsonflowersenescenceinseveralspecies[106],exogenousNOhasbeenshowntoreduceACO Antioxidants2019,8,167 9of22 activityandETemissionincutrose[115]. Therefore,similarlytoobservedinfruitripening,exogenous NOseemstonegativelyinfluenceETbiosynthesisinpostharvestcutflowers. WhetherNOactionis alsorelevantduringthenaturalsenescenceofflowerstriggeredbypollinationorageingremainsto beinvestigated. 3. NO–ETInterplayinAbioticStressResponses Environmentalstresses(e.g.,excesslight,cold,heat,salt,drought,flooding,nutrientdeficiencies, heavymetals)arerelevantdeterminantsofplantphysiologicalprocesses. Plantresponsestothese abioticstressesareregulatedbycrosstalkbetweenmultiplesignalmolecules,includingNOandET (Figure3). Antioxidants 2019, 8, x FOR PEER REVIEW 10 of 23 FFiigguurree 33.. SScchheemmaattiicc rreepprreesseennttaattiioonn ooff nniittrriicc ooxxiiddee ((NNOO))--eetthhyylleennee ((EETT)) iinntteerrppllaayy dduurriinngg aabbiioottiicc ssttrreessss rreessppoonnsseess iinn ppllaannttss.. AAbbbbrreevviiaattiioonnss:: AABBAA,, aabbsscciissiicc aacciidd;; AACCSS,, 11--aammiinnooccyycclloopprrooppaannee--11--ccaarrbbooxxyylliicc aacciidd ssyynntthhaassee,, AACCOO,, aammiinnooccyycclloopprrooppaannee--11--ccaarrbbooxxyylliicc aacciidd ooxxiiddaassee,, NNRR,, nniittrraattee rreedduuccttaassee;; HH22OO22,, hhyyddrrooggeenn ppeerrooxxiiddee;; RROOSS,r, eraecaticvtievoex yogxeyngespne csipeesc;ieexso; NexOo, eNxoOg, enexoougseNnOou;Hs MNsO,;h eHaMvysm, heteaalvs;y- Fme,eitraolns;d -eFfiec,i einrocyn; -dPe,fpichioesnpchy;o -rPu,s pdheofiscpiehnocryu;s- dMegfi,cmieangcny;e -sMiugm, mdeafigcnieesnicuym. deficiency. 3.1. NO–ETCrosstalkduringLightStressResponses 3.1. NO–ET Crosstalk during Light Stress Responses Lightnotonlyprovidesenergyforphotosynthesisbutalsorepresentsacrucialenvironmental Light not only provides energy for photosynthesis but also represents a crucial environmental signalresponsibleforadjustingplantgrowth,development,andreproduction. Processesasdiverseas signal responsible for adjusting plant growth, development, and reproduction. Processes as diverse seedgermination,seedlingde-etiolation,phototropism,flowering,fruitpigmentation,andentrainment as seed germination, seedling de-etiolation, phototropism, flowering, fruit pigmentation, and ofcircadianrhythmsareintrinsicallyregulatedbylightstimuli[116]. However,excesslightintensityand entrainment of circadian rhythms are intrinsically regulated by light stimuli [116]. However, excess UV-B-enrichmentcannegativelyimpactphotosyntheticefficiencybyinducingphotoinhibition,whichis light intensity and UV-B-enrichment can negatively impact photosynthetic efficiency by inducing linkedwithexcessivereactiveoxygenspecies(ROS)generation[108,117,118]. Incontrast,photosynthesis photoinhibition, which is linked with excessive reactive oxygen species (ROS) generation islimitedorhaltedwhenlightisabsentorbelowoptimallevels. Eitherway(excessiveorinsufficient [108,117,118]. In contrast, photosynthesis is limited or halted when light is absent or below optimal light)cantriggerchangesinbothNOandETmetabolism,aswellasinotherphytohormones[119]. levels. Either way (excessive or insufficient light) can trigger changes in both NO and ET metabolism, SignificantlyelevatedNOandETemissionsuponlightstresshavebeenfoundinArabidopsis[119]. as well as in other phytohormones [119]. Highlightintensity(555and1500µmolm−2s−1)andshorttimeofthelightexposure(2-4-6h)significantly Significantly elevated NO and ET emissions upon light stress have been found in Arabidopsis [119]. High light intensity (555 and 1500 µmol m−2 s−1) and short time of the light exposure (2-4-6 h) significantly increased NO emission in Arabidopsis shoot, but it was reduced under darkness after 12 h [119]. Moreover, high light exposure (500 µmol m−2 s−1) compared to the control illumination (70 µmol m−2 s−1) resulted in the attenuation of NOD activity and induced senescence in Arabidopsis thaliana by stimulating NR activity and enhancing NO emission [108]. Therefore, NO–ET interplay seems to positively influence high light-induced senescence but the interaction between the two gasotransmitters in light-stressed plants requires further attention. Similar to high light, UV-B radiation also results in significant ET and NO production in numerous plant species and organs [120,121]. NO–ET crosstalk in UV-B-stressed plants has been firstly evidenced by using chemical modulators [122]. Scavenging of UV-B-induced NO production using PTIO resulted in the repression of UV-B-triggered ET emission. At the same time, exogenous NO donor treatments (SNP) promoted the UV-B-induced ET accumulation in the seedlings. Authors Antioxidants2019,8,167 10of22 increasedNOemissioninArabidopsisshoot,butitwasreducedunderdarknessafter12h[119]. Moreover, highlightexposure(500µmolm−2s−1)comparedtothecontrolillumination(70µmolm−2s−1)resulted intheattenuationofNODactivityandinducedsenescenceinArabidopsisthalianabystimulatingNR activityandenhancingNOemission[108]. Therefore,NO–ETinterplayseemstopositivelyinfluence highlight-inducedsenescencebuttheinteractionbetweenthetwogasotransmittersinlight-stressed plantsrequiresfurtherattention. Similartohighlight,UV-BradiationalsoresultsinsignificantETandNOproductioninnumerous plantspeciesandorgans[120,121]. NO–ETcrosstalkinUV-B-stressedplantshasbeenfirstlyevidenced byusingchemicalmodulators[122]. ScavengingofUV-B-inducedNOproductionusingPTIOresulted intherepressionofUV-B-triggeredETemission. Atthesametime,exogenousNOdonortreatments (SNP)promotedtheUV-B-inducedETaccumulationintheseedlings. AuthorsconcludedthatNO couldpromoteETaccumulationunderUV-Bstress[122]. Also,stomatalclosureinducedbyUV-B radiationhasbeenreportedinViciafaba,whichwaspromotedbyNOaccumulationinguardcellsafter theETevolutionpeak[123]. BothUV-B-inducedNOgenerationandsubsequentstomatalclosurewere inhibitedbyNOscavengerandNRinhibitorsinguardcells. Atthesametime,exogenousNOdonor reversedUV-B-inducedstomatalclosureintheseplants[123]. Basedonthisobservation,EThasbeen implicatedasasignalactingupstreamNOduringUV-B-inducedstomatalclosure. Varioussignallingpathwayscanbefoundinvariousplantorgansandcelltypesuponpresence orabsenceoflight. ItiswellknownthatdarkstimulatesETproductionandstomatalclosurewhich ismediatedbyNO[124,125]. ApositivecorrelationbetweentheeffectsofETandNOonstomatal movementhasbeenobservedinthedark. BothethephonandACCreducedNOlevelsinguardcells of Vicia faba, thus promoting stomatal opening in darkness [126]. In addition, ACC and ethephon suppressedtheSNP-inducedstomatalclosureandNOlevelsinViciaguardcellsinthelight[127]. Incontrast,dose-dependentstomatalclosurehasbeenfoundafterETtreatmentunderlightcondition, which was mediated by NR-dependent NO accumulation in Vicia faba guard cells [128]. It can be concluded that depending on the light intensity ET induces stomatal opening or closure through influencingthelevelofNOinguardcells. 3.2. NO–ETCrosstalkduringTemperatureStressResponses Bothlowtemperature(coldandfreezing)stressandheatstresscanseriouslyaffectplantgrowth and development. Plants have evolved sophisticated mechanisms involving altered molecular, biochemicalandphysiologicalprocessestotoleratetemperaturestresses,inwhichETandNOarekey components,buttheirinteractionremainstobeelucidated[129,130]. TheNOdonorSNPhasbeenshowntoinducetheexpressionofMfSAMS1andresultedinan ◦ elevatedSAMlevel,PAconcentrationandPAoxidationundercoldstress(5 C)inMedicagosativa[131]. However,alteredETemissionhasbeenfoundinparallelwiththeenhancedtolerancetocoldstress. This reportindicatesthatSAMSplaysanimportantroleinplanttoleranceuponcoldstressviaup-regulating PAoxidationandimprovinghydrogenperoxide(H O )-inducedantioxidantprotection[131]. Although 2 2 itwasreportedthatNOincreasescoldtolerance,theroleofSAM,(acommonprecursorofPAandET) incoldstressisinnotwellunderstood. InlinewiththeabovedescribedantagonisticrelationshipbetweenET-NOduringfruitripening(see Section2.3),accumulatingevidencealsoindicatesacloseinteractionbetweenthesetwogasotransmitters infruitcoldstressresistance[81]. Forexample,treatmentswithdifferentdosagesofNOfumigation (5, 10, 20 and 40 µL L−1) significantly decreased ET production during fruit ripening after 2 and 4 weeks of cold storage, reduced chilling injury and delayed fruit colour development, as well as softeningandripeningincold-storedmangofruits[132]. SimilarchangeshavebeendescribedinYali pears(Pyrusbretschneideri),sinceETproductionandsolublesugarcontentdecreasedastheeffectof ◦ NOfumigationafter60daysat0 C,andthesofteningandripeningoffruitsweresimultaneously delayed[133]. OthershavealsofoundthatETandantioxidantenzyme(superoxidedismutase,SOD; CAT;peroxidase,POD)activitywasreducedafterNOfumigationinthe4-weekcold-storedpeach

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Abstract: Since their first description as atmospheric gases, it turned out that both nitric oxide. (NO) and ethylene (ET) are multifunctional plant signals.
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