ROS-mediated abiotic stress-induced programmed cell death in plants

16 Pages·2015·0.78 MB·English

by  Tsanko S. Gechev

REVIEWARTICLE
published:18February2015
doi:10.3389/fpls.2015.00069
ROS-mediated abiotic stress-induced programmed cell
death in plants
VeselinPetrov1,JacquesHille2,BerndMueller-Roeber3 andTsankoS.Gechev1,3*
1InstituteofMolecularBiologyandBiotechnology,Plovdiv,Bulgaria
2DepartmentofPharmacy,FacultyofMathematicsandNaturalSciences,UniversityofGroningen,Groningen,Netherlands
3DepartmentofMolecularBiology,InstituteofBiochemistryandBiology,UniversityofPotsdam,Potsdam-Golm,Germany
Editedby: Duringthecourseoftheirontogenesisplantsarecontinuouslyexposedtoalargevarietyof
PatrickGallois,Universityof abioticstressfactorswhichcandamagetissuesandjeopardizethesurvivaloftheorganism
Manchester,UK
unless properly countered.While animals can simply escape and thus evade stressors,
Reviewedby:
plantsassessileorganismshavedevelopedcomplexstrategiestowithstandthem.When
VasileiosFotopoulos,Cyprus
the intensity of a detrimental factor is high, one of the defense programs employed by
UniversityofTechnology,Cyprus
RobertFluhr,WeizmannInstituteof plants is the induction of programmed cell death (PCD). This is an active, genetically
Science,Israel controlled process which is initiated to isolate and remove damaged tissues thereby
*Correspondence: ensuring the survival of the organism.The mechanism of PCD induction usually includes
TsankoS.Gechev,Instituteof
anincreaseinthelevelsofreactiveoxygenspecies(ROS)whichareutilizedasmediators
MolecularBiologyandBiotechnology,
of the stress signal. Abiotic stress-induced PCD is not only a process of fundamental
RuskiBoulevard105,Plovdiv4000,
Bulgaria biologicalimportance,butalsoofconsiderableinteresttoagriculturalpracticeasithasthe
e-mail:[email protected] potential to significantly influence crop yield.Therefore, numerous scientific enterprises
havefocusedonelucidatingthemechanismsleadingtoandcontrollingPCDinresponseto
adverseconditionsinplants.Thisknowledgemayhelpdevelopnovelstrategiestoobtain
moreresilientcropvarietieswithimprovedtoleranceandenhancedproductivity.Theaim
of the present review is to summarize the recent advances in research on ROS-induced
PCDrelatedtoabioticstressandtheroleoftheorganellesintheprocess.
Keywords:abioticstress,programmedcelldeath,reactiveoxygenspecies,signaltransduction,stressadaptation
INTRODUCTION HO•,etc.)orexcitation(singletoxygen–1O )ofmolecularoxy-
2
Allorganismsneedtocopewithnumerousstressfactorsthrough- gen (Gechev etal.,2006) and are strong oxidizers that can react
outtheirlivesbyemployingawidevarietyofdefensivestrategies. with and damage a large variety of biological molecules (Petrov
Whilemobileindividualscaninmanycasesjustevadethem,plants andVan Breusegem,2012). They are regarded as byproducts of
assessilebeingshavedevelopedsophisticatedmorphological,bio- theaerobicwayoflifeandaregeneratedindifferentcellularcom-
chemical, and physiological adaptations in order to survive the partmentslikechloroplasts,mitochondriaandperoxisomes(Apel
detrimentaleffectsoftheenvironment(HirayamaandShinozaki, andHirt,2004).Despitetheirpotentialtoxicity,ROSactuallyhave
2010). To ensure proper and appropriate responses they have a dual role in vivo depending on their concentration, site and
evolved sensitive detection systems and robust signal transduc- durationofaction,previousexposurestostress,etc.(Milleretal.,
tionmechanisms.Moreover,thedifferentprotectivemeasuresare 2010).Ingeneral,lowerdosesofROSareemployedassignalsthat
triggeredinahighlyspecificandtightlycontrolledmannersothat mediateatleastpartoftheresponsestowardsstresswhileathigher
adequatereactionsareguaranteedwithoutanexcessivewasteof concentrationstheyposeasignificantthreatthatmayeventually
resources. lead to programmed cell death (PCD; Gechev and Hille, 2005;
Plants face two principle types of stresses, biotic and abiotic, Figure1).
both of which can be deleterious. A wide spectrum of bacteria, Programmed cell death is an active, genetically controlled
fungi, and viruses attack plants at various stages of their devel- processinwhichcellsareselectivelyeliminatedinahighlycoor-
opment and the severity of the biotic stress may be altered by dinated, multi-step fashion through the involvement of specific
abioticstresswhenitactsinparallelontheplant(Bostocketal., proteasesandnucleases. Thus,onlycellsthataredestinedtodie
2014). The latter includes extreme temperatures, high salinity, aredestroyedandnodamagetotheneighboringcellsisinflicted.
excessive light, water deprivation, pollutants such as ozone and Notably, PCD is central to a number of processes in non-stress
herbicides,highconcentrationsofheavymetals,excessiveUVradi- conditionslikethedifferentiationoftrachearyelements,thefor-
ation,andothers(GillandTuteja,2010).Acommonfeatureofthe mation of trichomes and root aerenchyma, abscission of floral
plants’responsestowardsallthesestressorsistheproductionof organs, embryo formation, shaping the morphology of certain
thesocalledreactiveoxygenspecies(ROS;JaspersandKangasjarvi, leaves,andmanyothers(Gadjevetal.,2008).Thebalancebetween
2010).Theseareformedbytheincompletereduction(hydrogen PCDandcellproliferation/elongationdeterminesthegrowthrate
•−
peroxide – H O ; superoxide radical – O ; hydroxyl radical – of plant tissues (Van Breusegem and Dat, 2006). Hence, PCD
2 2 2
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Petrovetal. ROS-mediatedabioticstress-inducedPCD
FIGURE1|AnoverviewofthecentralroleofROSintheresponses ROSsynthesis,previousstressexposure,developmentalstage,and
towardsabioticstressfactors.Differentabioticcueseitherdirectlyor interactionwithothersignalslikereactivenitrogenspecies(RNS)andCa2+
indirectly(throughtheactionofothersignalsandhormones)leadtothe arealsointegratedintotheresponse.Ingeneralrelativelyweakstressors
productionofROS.Inturn,ROSmayinfluenceavarietyofsignal causeonlyaslightriseinROSquantitieswhichleadstoadaptation.At
transductionsystems,thusprovidingpositiveornegativefeedbackcontrol moreintensiveabioticstimulithepriceforadaptationmaybeimpaired
mechanisms(redarrow).Thefunctionoftheantioxidantmachineryisto growthanddevelopmentoftheplant.Severestressusuallycauses
preventdangerouselevationsofROSlevels.TheoutcomeofROSsignaling massiveaccumulationofROSandtheinitiationofPCD,orinextreme
dependsmainlyontheROSconcentration,butotherfactorslikethesiteof casesevennecrosisofthetissue.
is vital for normal growth and development of plants. On the the mechanisms, like the induction of ROS production (Jaspers
other hand, PCD can be a consequence of severe abiotic and andKangasjarvi,2010),arecommonandoverlapbetweendiffer-
bioticstresses.Stress-inducedPCDsignificantlyaffectsplantyield ent kinds of abiotic cues (and even biotic stresses), some of the
andproductivityandisthereforeof fundamentalimportanceto utilizedsignaltransductionnetworks,recruitedtranscriptionfac-
agriculture(MittlerandBlumwald,2010). Thechangingclimate tors(TFs),andmodulatedgenesarespecificforeachkindofstress.
conditions,combinedwiththeexpandingWorld’spopulationand Moreover,recentevidenceshowsthatwhensubjectedtoacombi-
thelimitedpotentialtoincreasetheareaofarableland,hasdriven nationofmultiplestresses,plantsresponddifferentlythanwhen
both fundamental and applied research on stress responses and experiencingonlyasingletypeof stress(MittlerandBlumwald,
stress-inducedPCDwiththeultimategoaltominimizeyieldlosses 2010;AtkinsonandUrwin,2012).Thestudyofreactionstomul-
causedbyenvironmentalstresses(Cominellietal.,2013; Rosen- tiplestresseswillinthefuturebeofparticularinterest,sinceinthe
zweigetal.,2014).Theaimofthepresentreviewistosummarize fieldcropsareoftenconfrontedbyacombinationofdetrimental
the recent advances made in the field of abiotic-stress induced abioticfactors.
PCD and especially the roles of ROS as signaling mediators in
thisphenomenon.Genesinvolvedintheseprocessesarelistedin DROUGHTSTRESS-INDUCEDPCD
Table1;werefertomanyoftheminthefollowingtext. Drought is among the abiotic factors that most strongly affect
plantproductivityandcauseseriouslossestocropyield(Godfray
ROS-INDUCEDPCDAGAINSTPARTICULARABIOTICSTIMULI etal.,2010;TesterandLangridge,2010).Duringwaterdeprivation
Plants respond to specific abiotic stresses in a manner that energysupplyisseverelyrestrictedandROSbalanceisimpaired
depends on the identity of the stress factor. Although some of (Baena-Gonzalezetal.,2007;Milleretal.,2010).Notsurprisingly,
FrontiersinPlantScience|PlantPhysiology February2015|Volume6|Article69|2
Petrovetal. ROS-mediatedabioticstress-inducedPCD
Table1|ProteinsthatparticipateinthecontrolofPCDprocessesprovokedbydifferentabioticstresses.
Name Function/activity Relatedabioticstresses Reference
VPE,vacuolarprocessing APCD-executingprotease Salt,osmotic,heat,ER-stress Lietal.(2012),Mendesetal.(2013),
enzyme Kimetal.(2014)
BCL-2,B-celllymphoma2 SuppressorofVPE Salt,osmoticstress Kimetal.(2014)
AtCYSaandAtCYSb, Cysteineproteaseinhibitors Salt,drought,cold,oxidativestress Zhangetal.(2008)
cystatins
AtBOI,Botrytissusceptible1 UbiquitinatesBOS1,atranscription Saltstress Luoetal.(2010)
interactor factor(TF)implicatedinstress
responses
AtHSFA2,heatshockfactor Alleviatesoxidativestressduringheat Heatstress Zhangetal.(2009a)
A2 shock
mtHSP70,70kDaheat Maintains(cid:2)(cid:3)m Heatstress Qietal.,2011
shockprotein(HSP)
AtKOD,kissofdeath ApeptidethatinducesPCDresponses Heat,oxidativestress Blanvillainetal.(2011)
upstreamofmitochondrialdysfunction
AtMPK6,MAPkinase6 UpregulatesVPE,partofthe Heat,highUV,Cd2+-stress GonzalezBesteiroetal.(2011),Lietal.
UVR8-independentpathway,drives (2012),Jinetal.(2013)
responsestoCd2+
AtLSD1,lesionsimulating NegativeregulatorofPCD,interacts Cold,UV-C,high-lightstress Dietrichetal.(1997),Muhlenbocketal.
diseaseresistance1 withcatalases (2008),Huangetal.(2010),Wituszynska
etal.(2014),
AtDEAR1,DREBandEAR TranscriptionalrepressorofDREB Coldstress Tsutsuietal.(2009)
motifprotein1
AtMPK3,MAPkinase3 InvolvedintheUVR8-independent UVstress GonzalezBesteiroetal.(2011)
stresspathway
AtMC8,metacaspase8 ApartofthePCDpathwayprovokedby UV-stress Heetal.(2008)
UV-radiation
AtEDS1,enhanceddisease Controlsprocessesthatextinguish UV-C,highlightstress Muhlenbocketal.(2008),Wituszynska
susceptibility1 excessenergy,triacylglycerollipase etal.(2014)
AtPAD4,phytoalexin RegulatorinPCDpathwaycontrolledby High-lightstress Wiermeretal.(2005)
deficient4 LSD1,triacylglycerollipase
AtPARP,poly(ADP-ribose) SynthesizesADP-ribosepolymers, High-light,drought,heatstress DeBlocketal.(2005)
polymerase usingNAD+asasubstrate
AtNTL-4,TF EnhancesROSproductionduring Drought,heatstress Leeetal.(2012,2014)
drought-inducedsenescenceandheat
stress
AOX1a,alternativeoxidase MitigatesmitochondrialROSburst Alstress Liuetal.(2014)
1a
AtEXECUTER1and2 Driveseffectsafter1O2accumulation 1O2stress Leeetal.(2007)
AtSOLDAT,singlet Suppresses1O2-inducedcelldeath 1O2stress Colletal.(2009),Meskauskieneetal.
oxygen-linkeddeathactivator (2009)
AtANAC013,TF Conveysinformationabout Mitochondrialstress DeClercqetal.(2013)
mitochondrialdysfunction
AtbZIP28,TF TransducestheUPR-response;partof Heat,ERstress Liuetal.(2007),Gaoetal.(2008a)
theheatshocktolerancepathway
(continued)
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Petrovetal. ROS-mediatedabioticstress-inducedPCD
Table1|Continued
Name Function/activity Relatedabioticstresses Reference
AtbZIP60,TF TransducestheUPR-response; Salt,ERstress IwataandKoizumi(2005),Fujitaetal.
importantforsaltstresstolerance (2007)
AtNAC089,TF InducesER-triggeredPCD ERstress Yangetal.(2014)
GmNAC30andGmNAC81, SwitchonVPEexpressionafterERand Osmotic,ERstress Mendesetal.(2013)
TFs osmoticstress
BI-1,Bax-inhibitor1 AntiapoptoticproteinintheER ERstress WatanabeandLam(2006),Isbatetal.
(2009)
AtBiP2,ERluminalbinding ERchaperoneprotein,negative Cd2+stress Xuetal.(2013)
protein2 regulatorofPCD
AtTCTP,translationally InhibitsPCDprogression,probablyby Cold,salt,drought,Alstress Hoepflingeretal.(2013)
controlledtumorprotein sequesteringCa2+
AtUCP1,uncoupling Uncouplese−transportfromATP Salt,droughtstress Begcyetal.(2011)
protein1 synthesis
ZmABP9,ABREbinding ControlsABAsignalingandROS Drought,salt,coldstress Zhangetal.(2011)
protein9 accumulation
in the field drought usually occurs in combination with heat tolerance to paraquat and abiotic stress (Nishizawa etal.,2008).
•
andtheirsimultaneousactionhasasynergisticdetrimentaleffect Furthermore, both galactinol and raffinose can scavenge HO
onplantproductivity(Rampinoetal.,2012).Prolongeddrought invitro(Nishizawaetal.,2008).
stressisoftenassociatedwithROSaccumulation,mainlydueto An important physiological adaptation during drought is
decreasedCO fixationconcomitantwithincreasedelectronleak- the induction of leaf senescence. This process is executed by
2
agetotripletoxygenwhichmayeventuallyleadtoPCD(Gechev ROS-triggeredPCDinselectedleaveswhichallowsnutrientremo-
etal.,2012).FullyfunctionalROSdetoxifyingsystemsaretherefore bilization and an overall reduction of the transpiratory surface.
ofessentialimportanceforthetoleranceofplantstowardsdrought Thephytohormonesabscisicacid(ABA)andcytokininsalsocon-
anddesiccation(Kranneretal.,2002).Thereforeoneofthemain tribute to this phenomenon (Munné-Bosch and Alegre, 2004).
strategiestorestrictROSpropagationandavoidunnecessaryPCD RoottipmeristemsmayalsobeaffectedbyPCDasindicatedby
under drought is to reduce ROS formation by downregulating thedegradationoforganelles,anincreasedsizeofthevacuoleand
chlorophyllsynthesisandothercomponentsofthephotosynthetic plasmalemmacollapseduringdehydrationinArabidopsisthaliana
machinery(Farrantetal.,2007).Anotherfactorthatcontributes (Duanetal.,2010).Thisisanadaptivemechanismthatisswitched
toproperprotectionintheseconditionsisawell-balancedsucrose on to promote the development of lateral roots with enhanced
metabolism(Liuetal.,2013b). Sucrosefuelstheglycolyticpath- stresstolerancewhichareimportantforpost-stressrecovery.
waywhichinturnfeedstheoxidativepentosephosphatepathway. A prominent problem that occurs during periods of water
The latter produces reducing power (NADPH) which is needed deficit and other abiotic stresses is microspore abortion result-
forthesynthesisof manynon-enzymaticantioxidantsincluding ing in male sterility, which is due to the extreme sensitivity of
glutathione, ascorbic acid and flavonoids that are able to scav- themalereproductiveprogramtoadverseenvironmentalcondi-
engeROS(Bolouri-Moghaddametal.,2010). Insupportof this tions.ThismaybeattributedtotheincreaseinROSconcentrations
hypothesis comes the finding that in two different cultivars of following periods of drought and the subsequent PCD of the
soybean the activities of glucose-6-phosphate dehydrogenase, a microspores(DeStormeandGeelen,2014). Forexample, when
centralenzymeofthepentosephosphatepathway,correlatewith riceanthersareexposedtoashort-termdroughttreatmentaccu-
activitiesoftheantioxidantenzymesglutathionereductase(GR), mulation of H O is observed, accompanied by a reduced level
2 2
moodehydroascorbate reductase (MDHAR), and dehydroascor- of transcripts of antioxidant enzymes as well as ATP depletion.
bate reductase (DHAR; Liu etal., 2013a). Sucrose as well as AllthesechangesultimatelyleadtoPCDindevelopinganthersas
raffinosefamilyoligosaccharides,whichaccumulateduringdehy- confirmedbyDNAfragmentationinthesetissues(Nguyenetal.,
dration,canalsoactascompatiblesolutestoprotectfromdrought 2009).
stress(Farrantetal.,2007). Inaddition, galactinolandraffinose EndogenousABA,which regulates stomatal closure and thus
candirectlyprotectplantsfromoxidativestressasshowninAra- CO uptake,rapidlyaccumulatesduringperiodsof waterdepri-
2
bidopsisplantsoverexpressinggalactinolsynthasewhereelevated vation (Osakabe etal.,2014). The signaling pathway stimulated
levels of galactinol and raffinose correlated with an increased byABAinguardcellsatfirstleadstoaboostofROSproduction,
FrontiersinPlantScience|PlantPhysiology February2015|Volume6|Article69|4
Petrovetal. ROS-mediatedabioticstress-inducedPCD
which in turn provokes an increase in the cytosolic Ca2+ con- AtCYSa andAtCYSb – was shown to improve the tolerance not
+
centration.Subsequently,activationofanionandK effluxfrom onlytosaltstress,butalsotodrought,coldandoxidation(Zhang
thecellthroughspecificionchannelsresultsinthereductionof etal.,2008).
the guard cell turgor and thereby stomatal closure (Kwak etal., Mitochondriaplayapivotalroleinsalt-inducedPCDinplants,
2003).Thisprocess,however,isanexampleofabeneficialfunc- especiallyinnon-photosyntheticcells.Thereasonisthatinthese
tionofROSwhichdoesnotnecessarilyculminateinPCD.Another tissuesmitochondriaarethemainROS-producingcompartment.
droughtstressresponsemechanisminwhichABAisimplicatedis TheROSburstinmitochondriamayleadtoalossofoutermem-
thereorientationofpolyamine(PA)metabolismincertainspecies branepotential,whichisanearlymarkerforPCDinA.thaliana
like grapevine. In this case ABA induces PA accumulation and (Yaoetal.,2004).Indeed,intobaccoprotoplastssubjectedtosalt
extrusion to the apoplast, where the PAs are then targeted by stress,thePCDprogramismediatedbyROSanddependsonthe
apoplasticamineoxidases. Oneof theproductsof thefollowing openingofthemitochondrialpermeabilitytransitionpores(PTP;
reactionisH O ,whichmayorchestratefurtherstressresponses Linetal.,2006).
2 2
orinducePCDwhenpresentinhighconcentrations(Toumietal., SinceexcessiveROSproductionswitchesonthePCDprogram
2010). andmayjeopardizethesurvivaloftheplant,manyoftheresponses
towardsabioticstresses,includinghighsaltconcentrations,aimat
SALT/OSMOTIC-STRESSINDUCEDPCD minimizing the ROS threat. This is usually achieved by a very
ThiskindofstressincreasesROSconcentrationsandpossiblyleads tightcontroloftheantioxidantsystemsandupregulationofdif-
to PCD by different mechanisms. In C3 plants the main source ferentantioxidants,bothenzymaticandnon-enzymatic.Agood
of ROS is the accelerated rate of photorespiration, which con- exampleisthehalophyticshrubProsopisstrombuliferawhichafter
tributes to up to 70% of the accumulated H O (Noctor etal., treatmentwithNa SO boostsantioxidantactivities,thesynthesis
2 2 2 4
2002).InC4andCAMplantsphotorespirationproceedsinaneg- offlavonoidcompoundsandincreasesthecarotenoid/chlorophyll
ligiblepace,whichmakesthechloroplastelectrontransportchain ratio(Reginatoetal.,2014).AnothermechanismtokeepROSlev-
themainROSproducer.Moreover,duringosmoticstressNADPH elsundercontrol,whensubjectedtosaltstress,istheaccumulation
oxidasesandapoplasticdiamineandPAoxidasesareactivatedasis ofcompatiblesolutes.Theseorganicosmolytesareneededtokeep
mitochondrialrespiration,whichfurtherelevatesROSconcentra- proper osmotic potential in stressed tissues but contribute also
tion(Abogadallah,2010).NADPHoxidase-producedsuperoxide byalleviatingoxidativestress(Liuetal.,2011;Duanetal.,2012).
anionsarenecessaryfortheexecutionofaPCDprogramswitched Interestingly,recentexperimentsperformedwithbarleyandwheat
onbybothNaClandsorbitolintobaccocells(Monettietal.,2014). demonstrated that the rise in compatible solute concentrations
However, the molecular reactions following the ionic NaCl and provides cross-tolerance also to UV-B stress (Puniran-Hartley
non-ionicsorbitoltreatmentsdonotcompletelyoverlap(Monetti etal.,2014).Thus,despitebeingmetabolicallyexpensiveinterms
etal.,2014)whichsuggeststhattheseresponsesarehighlyspecific. of required energy and carbon input, the salt-induced de novo
PAoxidasescontributedirectlytotheH O loadintheapoplast synthesisofcompatiblesolutesmayservemultiplepurposesand
2 2
since they catabolize PAs like spermidine, which are extruded improve the chances of survival in hostile environments which
into the apoplasts under high salinity, and produce H O as a poseacombinationofabioticchallenges.Theintegrityofantioxi-
2 2
byproduct(Moschouetal.,2008). Salinity-provokedPCDisnot dantsystemsisofvitalimportanceforseedsaswell.Theirabilityto
restricted to higher plants, as demonstrated by Affenzeller etal. germinatedependsontheROSstatusandacompromisedantiox-
(2009),whoreportthisphenomenoninthefreshwatergreenalga idantmachinery,especiallyincombinationwithabioticstresses,
Micrasteriasdenticulata. maysignificantlyreducegerminationefficiency. Suchisthecase
Animportantfeatureofsalt-inducedPCDisthatitisstrongly inA.thalianaseedswhichlackthecytosolicantioxidantASCOR-
affected by ion disequilibrium and may be the result of inva- BATEPEROXIDASE6whensubjectedtosaltandheatstress(Chen
+ +
sionof Na intothecytosolaccompaniedbyadeficiencyof K etal.,2014).
+
(Kim etal., 2014). The efflux of K is influenced by hydroxyl
radicalsandinturnregulatesdifferentenzymesinvolvedinPCD EXTREMETEMPERATURE-INDUCEDPCD
(Demidchiketal.,2010).Thesefindingssuggestthatmaintenance Hightemperaturessignificantlyaffectplantgrowthanddevelop-
+ +
of ionic homeostasis and proper Na /K ratios could be used mentbytriggeringmassivemetabolic,physiological,andgenetic
to manipulate salt stress tolerance in crops (Huh etal., 2002; reprogramming. Like other abiotic stress factors, heat shock is
Teakle and Tyerman,2010). For example, a recent study in rice knowntoinducePCD(Vaccaetal.,2004). Tobaccocellstreated
demonstratedthatBCL-2,anantiapoptoticprotein,canregulate with high temperatures produce drastically larger quantities of
vacuolarprocessingenzymes(VPE),whichplayacrucialrolein ROS.TheseareaprerequisiteforasuccessfulPCDsinceaddition
manyPCDprocesses, bymodulatingionfluxes. Overexpression of theantioxidantsascorbateorsuperoxidedismutase(SOD)to
+
ofBCL-2significantlyreducesNaCl-inducedK efflux,represses the cultures supports cell survival. Moreover, the authors show
•−
theexpressionofVPEsandthusalleviatesPCDsymptoms(Kim thatbothH O andO arerequiredandtheabsenceofeitherof
2 2 2
etal., 2014). A detailed model of the ion-specific signaling that themcompromisesthePCDprocess. Mitochondriaalsoplayan
+
triggersPCDunderhighNa concentrationshasbeenproposed importantroleintheseconditions.Theyreleasefunctionallyactive
by Shabala (2009). Another mode of modulating the stress and cytochromecinaROS-dependentmanner,whichcontributesto
PCDresponsesisthroughcysteineproteaseinhibitors(cystatins). theactivationofcaspase-likeproteasesinthecytosolthatexecute
For instance, the overexpression of two Arabidopsis cystatins – thePCDprogram(Vaccaetal.,2006).Anewerstudydemonstrates
www.frontiersin.org February2015|Volume6|Article69|5
Petrovetal. ROS-mediatedabioticstress-inducedPCD
thatPCDistriggeredonlywhenthetemperaturerisesaboveaspe- are targeted to the vacuole, where they are activated to pro-
cificthresholdwhichisassociatedwithmetabolicchangesthatare cess a number of vacuolar hydrolases and proteases associated
considerablydifferenttothoseinresponsetolessintensivestimuli withPCD.
(Marsoni etal., 2010). For example, only in severe heat shock- Amongthemajorsitesof ROSproductionduringheatshock
treatedcellsisadownregulationofantioxidantproteinsobserved. is the photosynthetic apparatus. As a consequence of high tem-
Thisinturnleadstotheperturbationoftheredoxhomeostasisand perature the photosystem II complexes (PSII) may be severely
playsaroleinthePCDevents.Whensubjectedtoshorterorless damagedduetocofactordissociation.Thishasnumerouseffects,
intensiveheatstimuliplantscanbecomeprimedandthusmore one of which is the formation of ROS (Mathur etal., 2014).
resistant to subsequent stressful events. This enhanced thermo- Elevated concentrations of H O may also be generated in per-
2 2
toleranceisachievedbyanimprovedantioxidantcapacity,which oxisomes due to photorespiratory activity which is significantly
inwheatseedlingsisbasedonupregulatedexpressionandhigher acceleratedatelevatedtemperatures.Thereasonisthereduction
activities of SODs, GR,and peroxidases (Wang etal.,2014) and of the relative specificity of ribulose-1,5-bisphosphate carboxy-
onceagainconfirmstheimportanceofROShomeostasisforplant lase/oxygenase(RuBisCO)forCO comparedtoO andthelower
2 2
performance under these conditions. An interesting fact is that relative solubility of CO than O (Jordan and Ogren, 1984).
2 2
proline, which acts as a compatible solute, ROS detoxifier and However, the shift of H O production from chloroplasts to
2 2
regulator of the redox balance (Szabados and Savoure,2010), is peroxisomesduetophotorespirationcanberegardedaslessdan-
inhibitory to Arabidopsis seedlings during heat stress (Lv etal., geroussinceperoxisomesarebettersuitedtocopewiththeH O
2 2
2011).Thisisincontrasttotheroleofprolineforothertypesof loadmainlyduetotheabundanceofthereductant-independent
stresses,especiallysalt/osmoticstress,whereithasaprotectiverole enzymecatalase(Wingleretal.,2000).
(VerbruggenandHermans,2008).Thesefactssupportthenotion Lowtemperature(bothchillingandfreezing)onitsowncan
thateverytypeofabioticinfluencetriggersaspecificsequenceof also induce PCD in plants (Koukalova etal.,1997; Lyubushkina
adaptivereactions. etal.,2014).TobaccoBY-2suspensioncellsprogressivelydevelop
An important detail is that the type and localization of ROS characteristicfeaturesofPCD,includingDNAcondensationand
◦
may influence the execution of the PCD program that follows. fragmentation (laddering), after exposure to 5–6 C for two to
Recently it was observed that the exogenous application of the 5 weeks (Koukalova etal., 1997). Interestingly, 11% of the cells
unspecificantioxidantsascorbateandglutathionetoheat-treated did not die even after prolonged incubation at low tempera-
A. thaliana cells actually favors the initiation of PCD, probably ture. Winter wheat (Triticum aestivum L.) cell cultures exposed
because cellular stress levels are reduced and the uncontrolled tofreezingtreatment(−8◦C)undergoPCDaccompaniedbyROS
necrotic death is avoided. In contrast, treatment with catalase, accumulation,DNAfragmentation,andthereleaseofcytochrome
whichisspecificonlyforH O ,temporarilysuppressesPCD.The cfrommitochondriaintothecytosol(Lyubushkinaetal.,2014).
2 2
authorshypothesizethatitistheH O whichmayfunctionasthe LESION SIMULATING DISEASE RESISTANCE 1 (LSD1) is a
2 2
PCD-inducingmobilesignal,whiletheothertypesofROSandthe plant-specificnegativeregulatorofPCDanditsmutationcauses
productsof theiractivityserveaspositiveornegativeregulators ROSaccumulationandrunawaycelldeath(Jabsetal.,1996;Diet-
of the components of the PCD machinery (Doyle and McCabe, rich etal.,1997). LSD1 interacts with catalases inA. thaliana to
2010). keep ROS under control and loss of its function renders plants
It has been proposed that heat shock transcription factors moresusceptibletolowtemperature-inducedcelldeath(Huang
(HSFs), which are central to the coordinated expression of heat etal.,2010;Lietal.,2013).
shock proteins (HSPs) and other stress-related genes, have an Lowtemperatureisparticularlydamagingwhencombinedwith
important role in the ROS-mediated response to heat stress elevatedlightintensities. Duringsuchconditions,thephotosyn-
becausetheymayfunctionasROS-sensitivesensors(Millerand theticelectrontransportchainsareoverreduced,thereisincreased
Mittler,2006).Both,theHSF andHSP genesarehighlyinduced generationofROS,andtheantioxidantsystemcannotcopewith
byROS(Gechevetal.,2005;Piterkovaetal.,2013).LackofHSFA2 it. Asaresult,photoinhibitionor/andcelldeathoccurs(Murata
causes accumulation of higher ROS levels, more severe mito- etal.,2007).
chondrialdysfunctionandalowersurvivalrateduetoincreased
PCD (Zhang etal., 2009a). In rice, overexpression of the mito- UVLIGHT-INDUCEDPCD
chondrial HSP mtHSP70 may suppress the PCD response at TheUVspectrumcomprisesthreerangesofdifferentwavelengths:
elevatedtemperaturesandafterH O treatmentbymaintaining UV-A (315–390 nm), UV-B (280–315 nm) and UV-C (below
2 2
themitochondrialtransmembranepotential((cid:2)(cid:3)m)andreduc- 280 nm). Of these, UV-C is often used as a reliable trigger of
ingROSamplification(Qietal.,2011).Othercomponentsofthe PCDinscientificstudies(Gaoetal.,2008b)despitethefactthat
molecular machinery transducing the heat shock signal include innaturalconditionsUV-Cisabsorbedbytheozonelayerinthe
the mitogen-activated protein kinase 6 (MPK6) and γVPE (Li stratosphereandisthereforeoflittlephysiologicalrelevance.UV-B
etal.,2012).Accordingtothisstudy,thecascadethatistriggered exposure, in turn, has been widely considered as a potent stres-
at elevated temperatures starts with the accumulation of ROS sor of plants in the past, but in the last years this concept has
and an increase of the cytosolic Ca2+ concentration. Calcium beenreconsidered(Hidegetal.,2013)sincemanystudiesfailedto
in turn is bound by a form of the ubiquitous second messen- demonstratedirectevidenceforUV-Bprovokedstressinterrestrial
ger calmodulin (CaM3) which leads to the activation of MPK6. ecosystems(Ballareetal.,2011).Itwasproposedthatlow,ecolog-
Finally,MPK6upregulatesγVPEexpressionandγVPEprecursors icallyrelevantUV-Bdosesinducesocalled“eustress,”acondition
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Petrovetal. ROS-mediatedabioticstress-inducedPCD
that primes the plant for future oxidative pressure but does not ROS homeostasis (Wituszynska etal., 2014). In mitochondria,
impedegrowthanddevelopmentperse,whilehighUV-Binten- which are affected by UV-C, a ROS burst leads to a decline in
sity leads to a state of“distress”which is associated with a ROS the (cid:2)(cid:3)m. Other symptoms of the mitochondrial dysfunction
burst and may eventually result in PCD (Hideg etal.,2013). In include changes of their distribution and mobility (Gao etal.,
experimentalconditionstheUV-Birradiationthatisusedisusu- 2008b). The rise of ROS quantities and the damage to mito-
ally strong enough to overload the antioxidant capacities of the chondria are important for the normal completion of a PCD
cellsandcauseoxidativestress. programasindicatedbythefactthattreatmentwiththeantiox-
Strong UV light has been shown to be deleterious to both idant ascorbic acid or the inhibitor of the mitochondrial PTPs,
animals and plants. In animals it causes apoptosis (Kulms and i.e. cyclosporine, reduces the rate of PCD. In summary, ROS
Schwarz,2000)whileinplantsitleadstoapoptotic-likesymptoms that mediate the signal for PCD after UV-C treatment mainly
likeDNAladderingandfragmentationofthenucleus(Danonand originate in mitochondria and chloroplasts as described above,
•−
Gallois,1998).ThisabioticcueleadstoasharpriseinO concen- which in normal physiological conditions are in close proxim-
2
−
trationsinchloroplastsduetoe excitationbyenergytransition ity to allow metabolic interchange (Logan and Leaver, 2000).
in different photosensitizers (Hideg etal., 2002). The plastidic Moreover, light is also necessary for this type of PCD to occur
•−
SODscantransformO toH O whichisanotherconsequence as well as caspase-like activities as demonstrated by the ability
2 2 2
of UV stress. In Rosa X damascena (the Damask rose) the peak of caspase inhibitors to impede the process (Danon etal.,2004;
of H O accumulation is 60–90 min after irradiation (Murphy Zhangetal.,2009b).
2 2
and Huerta,1990). Recently, it was shown that in UV-B irradi-
atedtobaccoleavestheantioxidantactivitiestargetingH2O2 are HIGHLIGHT-INDUCEDPCD
the most activated (Majer etal.,2014). This suggests that H O Light with intensity higher than 1000 μmol photons m−2s−1
2 2
scavengingwouldbecrucialforsurvivalinsuchconditions.Inter- can be very damaging to plants and especially to chloroplasts
estingly,itwasshownbyexperimentswithfluorescentsensorsof (Szechynska-Hebda and Karpinski, 2013). In these conditions,
different ROS forms that the relative portion of 1O formed as leading to excess excitation energy (EEE), leaves are exposed to
2
aresultof UVtreatmentislowincomparisontotheotherROS more energy than they can actually utilize in photosynthesis or
(Hideg etal., 2002). To prevent PCD, high UV-B doses trigger dissipatewithoutbeingharmed(WilhelmandSelmar,2011).The
adefenseprogramaimingtoalleviatethesymptomsofoxidative enzymaticprocessesofCO fixationareslowed,whichisaccom-
2
stressincludingsynthesisofthestresshormonessalicylicacid(SA), paniedbythesynthesisofhigherthannecessaryconcentrationsof
jasmonic acid (JA),and ethylene, upregulation of pathogenesis- NADPHandATP.Theincreaseinreducingequivalentsreducesthe
related proteins and genes participating in senescence processes plastoquinonepooland/orinhibitstheoxygenevolutioncomplex
(Bandurska etal., 2013). Stress avoidance and stress tolerance responsibleforthephotolysisofwater.AsaresultthePSIIcom-
strategies induce morphological changes and adaptations of the plexesareinactivated,aprocessknownasphotoinhibition,which
metabolismtofavortheaccumulationofflavonoidsinepidermal goeshandinhandwithphotoreductionof molecularoxygento
cells, lignindepositionincellwalls, andtoreinforcetheantiox- ROS(Andersonetal.,1997).Iftheantioxidantsystemsfailtokeep
idant system with both enzymatic (SOD, catalase, peroxidases) ROSpropagationundercontrol,growthretardationandPCDmay
and non-enzymatic ROS scavengers (carotenoids, tocopherols, occur(Mateoetal.,2004).ExamplesofthedamagethatROScan
ascorbicacid,PAs,etc.; UedaandNakamura,2011; Zhangetal., cause in these conditions include the degradation of glutamine
2012). synthetase,phosphoglycolatephosphatase,andthelargesubunit
Two independent UV-B response pathways were proposed to ofRuBisCOaswellastheincreasedoccurrenceofcarbonylgroups
actinaccordancetotheUV-Bfluencerate(Nawkaretal.,2013). instromalproteins(StiegerandFeller,1997).
The UV RESISTANCE LOCUS8 protein (UVR8), characterized Plantsreactwithacomplexadaptivesystemicacquiredacclima-
asamajorUV-Bphotoreceptor(Kliebensteinetal.,2002;Rizzini tionresponse(SAA)towardsEEE.Recentlyithasbeenshownthat
etal., 2011), mediates photomorphogenic adaptive responses to SAAandPCDsignalsareregulatedbystomatalconductance,pho-
moderate levels of UV-B. To achieve this UVR8 interacts with torespiration,ROShomeostasis,hormonalbalanceaswellaslocal
theCONSTITUTIVEPHOTOMORPHOGENESIS1(COP1)pro- changes in the plasma membrane electric potential called pho-
tein and induces the TFs ELONGATED HYPOCOTYL (HY5) toelectrophysiological signaling (PEPS; Szechynska-Hebda etal.,
and HY5 HOMOLOG (HYH; Brown and Jenkins, 2008). In 2010).ThepropagationofEEE-inducedPCDinitiatedbychanges
contrast, high fluence rates trigger a stress UVR8-independent intheredoxstateof thechloroplastsisdependentontheactivi-
pathwaythatincludesamitogen-activatedproteinkinase(MAPK) tiesofseveralregulatorygeneslikeLSD1,EDS1,PHYTOALEXIN
cascadeinvolvingtheantagonisticactionofMAPKINASEPHOS- DEFICIENT 4 (PAD4) and ETHYLENE INSENSITIVE2 (EIN2),
PHATASE 1 (MKP1) and the MAP-kinases MPK3 and MPK6 whose protein products function upstream of ROS production
(GonzalezBesteiroetal.,2011). (Muhlenbocketal.,2008;Karpinskietal.,2013).
The LSD1 and ENHANCED DISEASE SUSCEPTIBILITY 1 Plantswithcompromisedantioxidantsystemsorpropercom-
(EDS1)proteinsareantagonisticregulatorsoftheacclimationto positionofthephotosyntheticmachineryhavebeenwidelyused
UV-C stress, since lsd1 mutants are characterized by enhanced tostudythePCDresponsestriggeredbymassiveROSaccumula-
cell death after UV-C treatment, while eds1 plants manifest tionprovokedbyexcessivelight. Forexample,experimentswith
the opposite phenotype. They exert their function by control- theArabidopsis mutantsvte1npq1, deficientinα-tocopheroland
lingtheprocessesthatextinguishexcessiveenergyandmodulate zeaxanthin,andch1,lackingchlorophyllb,havedemonstratedthat
www.frontiersin.org February2015|Volume6|Article69|7
Petrovetal. ROS-mediatedabioticstress-inducedPCD
theriseofthe1O concentrationsfollowinghighlighttreatment Aluminum(Al)isanotherhighlytoxicelementwhichcauses
2
candirectlyleadtoPCDduetothecytotoxicityof1O (Trianta- damagetobothanimals,includinghumans,andplants.Alnega-
2
phylidesetal.,2008).Interestingly,thech1mutantcanberescued tivelyaffectsthesoil-derivedwaterandnutrientsupplyinplants
from this 1O -dependent PCD if subjected to mild light stress byinhibitingthedivisionandelongationofroottipcells(Samac
2
acclimationfirst(Rameletal.,2013).However,inanothermutant, and Tesfaye, 2003). ROS burst, mitochondrial dysfunction, and
npq1lut2, which is unable to produce the 1O quenchers lutein induction of PCD are considered to be the main symptoms of
2
and zeaxanthin, 1O responses did not include PCD (Alboresi exposure to Al at the cellular level (Li and Xing, 2010). The
2
etal.,2011),suggestingthattheidentityof1O -inducedreactions sequenceofeventsintheseconditionsincludesstimulationofROS
2
underhighlightdependsonthesourceof1O inthechloroplasts synthesis,forexamplebyadramaticupregulationoftheO•−pro-
2 2
andtheintensityofthesignal.H O hasalsobeenshowntoini- ducerrespiratoryburstoxidasehomolog(Rboh),openingof the
2 2
tiatePCDinexcessivelylight-stressedplants(Vandenabeeleetal., mitochondrialPTP,reducedpotentialoftheinnermitochondrial
2003;Mullineauxetal.,2006). membrane,releaseofcytochromecintothecytosolandfinally–
anactivationof thecaspase-like3protease(Huangetal.,2014).
HEAVYMETAL-INDUCEDPCD Interestingly, the PCD features are relieved after the application
Itiswell-knownthathighconcentrationsofheavymetalionscan ofproteaseandhumancaspaseinhibitors,whichsuggestsinvolve-
stimulateaROSburst(Datetal.,2000;ChoandSeo,2005).Evi- mentofcaspase-likeproteasesinthecelldeathprocess.Asimilar
denceforthisistheincreasedlipidperoxidationinplantssubjected celldeath-suppressioneffectisobservedafteradditionofantiox-
to heavy metal stress. For example, after treatment of Solanum idants like catalase, ascorbic acid and its precursor L-galactonic
nigrumwithcadmium(Cd),malondialdehydeaccumulates,indi- acid-γ-lactoneaswellascompoundsknowntointeractwithand
cating augmented oxidation of membrane lipids by ROS (Deng inhibitNADPHoxidases(Yakimovaetal.,2007),whichonceagain
etal.,2010).Oneshouldalsokeepinmindthatsomeheavymet- confirmstheimportanceofROSforAl-inducedPCD.Themito-
als,likeFeandCu,mayparticipateintheHaber–Weissreaction chondrialenzymealternativeoxidase(AOX),whichisspecificfor
whichleadstotheproductionofthehyper-activehydroxylradical plantsandservestopreventover-reductionofthemitochondrial
•−
(HO ;Kehrer,2000). electron transport chain, is also involved inAl stress as demon-
ManyreportsstudyPCDinducedbydifferentheavymetalions. stratedrecently(Liuetal.,2014).Accordingtothisstudy,AOX1a
•−
Cd,forexample,appearstotriggerPCDbyapathwaythatinvolves upregulationisprovokedbyAl-derivedO inthemitochondria
2
the endoplasmatic reticulum (ER), in which unfolded proteins andAOX1ainturncanmitigatethefollowingPCDbymaintaining
accumulate(Xuetal.,2013).ThishasbeendemonstratedinNico- propermitochondrialfunctions.
tianatabacumBY-2cellsinwhichmarkersforERstress(NtBLP4 Tungsten(W)isnotasabundantasAlandCd,butitsquan-
andNtPDI)wereupregulatedafterexposuretoCd,whilechemical tities can be augmented as a result of human activities. Like
andprotein(expressionof theArabidopsisAtBiP2gene)chaper- other heavy metals, W is also harmful, with a negative impact
onescansuppressthisinduction,aswellastheinductionof the onplantgrowthcausedbybindingtoandinactivationofmolyb-
PCD-related gene NtHsr203J. Ethylene, which is modulated by doenzymes and switching on PCD. The cell death initiated by
ROSformation,alsoparticipatesinthereactionsofplantstoCd high W concentrations has been studied in pea root cells and
stresssinceitstimulatestheonsetofPCD(Yakimovaetal.,2006; according to the results the mechanism involves the ER, sim-
Liuetal.,2008).ItappearsthatthecellularresponsetoCdinvolves ilar to Cd (Adamakis etal., 2011). A possible explanation for
complexcrosstalkbetweenROS,NO,Ca2+ ions,andhormones. the effect of the inhibitory role of W on molybdoenzymes and
Inastudywithpeaplantsitwasshownthatoneof theprimary the activation of ROS-dependent PCD came from the obser-
effectsofCd2+ treatmentisactuallydepletionofcytosolicCa2+ vation that the xdh1 mutant of A. thaliana, which is deficient
whichnegativelyregulatescomponentsoftheantioxidantsystem for the molybdenum-containing enzyme xanthine dehydroge-
•−
likeSOD.ThisresultsinelevatedH O andO concentrations. nase,accumulatedxanthineandexhibitedsymptomsofpremature
2 2 2
Ontheotherhand,thereductionofCa2+affectsalsoNOproduc- senescence(Brychkovaetal.,2008).Furthermore,thexdh1mutant
tion,leadingtoitsdepression.ButthedecreaseinNOcaninturn subjectedtodarknessandsubsequentre-exposuretolightaccu-
•−
promotetheaccumulationofO ,furtherexacerbatingtheoxida- mulated ROS and exhibited cell death to a larger extent than
2
tive load. The lipid peroxidation in membranes caused by ROS the wild type, an effect that could be attenuated by the addi-
turnsonJAandethylenemediatedpathways(Rodriguez-Serrano tion of allantoin or allantoate, indicating that these metabolites
etal.,2009).Manygenesundergoexpressionchangesinsuchcon- protect cells from cellular damage by ROS (Brychkova etal.,
ditions,includingelementsofMAPKcascadesaswellasenzymes 2008).
involved in ethylene, NO and PA metabolism (Kovalchuk etal., Unlikethenon-essentialmetalslikeAl,W,andCdmentioned
2005; Chmielowska-Bak etal., 2013). The relationship between above, some other metallic elements, such as zinc (Zn), are
CdandoxidativestressesmanifestsalsoinexperimentswithAra- important micronutrients with an array of functions. Although
bidopsismutantswhicharecharacterizedbytolerancetobothof Zndeficiencyhasmanynegativeconsequencestoplants,includ-
them.Suchisthecaseforplantsoverexpressinganaldehydedehy- ing growth retardation and reduction of the efficiency of the
drogenase(ALDH3;Sunkaretal.,2003),mutantsofaMAP-kinase antioxidant system (Sharma etal.,2004), accumulation of Zn is
(mpk6; Jin etal., 2013) and the atr lines which are less sensi- highlydeleterious(Wangetal.,2009).ThemechanismsofZntox-
tivetoCd-andparaquat-inducedoxidativestress(Radevaetal., icityhavenotbeenfullyelucidatedyet,butsimilartootherheavy
2010). metals the symptoms involve a ROS imbalance and ultimately
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Petrovetal. ROS-mediatedabioticstress-inducedPCD
may lead to PCD. In a study with Solanum nigrum roots it was toallowtheemergenceofadventitiousrootsinriceasaresponse
demonstratedthatZn2+initiallyboostsNOproductionandNO toflooding(Steffensetal.,2012).
inturnnegativelyregulatescomponentsoftheantioxidantsystem As in other cases of abiotic stress-induced PCD, the reactive
therebyincreasingROSconcentrationsandtriggeringPCD.The nitrogenspecies(RNS)NOmayalsoplayaroleduringexposure
riseof NOwasproventobenecessaryforthisZn-inducedPCD to low oxygen levels. NO is mainly produced in mitochondria,
sinceitsinhibitionpreventedROSaccumulationandthesubse- mostlybythereductionofnitritebytheelectrontransportchain
quent cell death (Xu etal., 2010). Interestingly, Zn participates (GuptaandIgamberdiev,2011).Importantly,anegativefeedback
alsoinbeneficialPCDprocessesthroughoutplantdevelopment. loop between ROS, NO, and AOX was found to exist in mito-
InNorwayspruce(Piceaabies)somaticembryosZnmanifestsan chondria;NOisabletoactuallyinduceAOXexpression,probably
anti-cell death effect and is contained (in physiological concen- to reduce the ROS and NO burden (Fu etal., 2010). Although
trations) within the proliferating cells, while those that need to this mechanism is supposed to keep ROS and NO concentra-
be subjected to PCD are Zn-depleted (Helmersson etal.,2008). tions under control, it may be overrun by ROS and NO from
Allthesefindingsconfirmthatinthecaseof Znthedosemakes non-mitochondrialorigininwhichcasePCD,causedbytheROS
thepoisonanddisruptionofitshomeostasisineitherdirection- and NO accumulation, may occur (Gupta etal., 2012). During
depletionoraccumulation–canhavedramaticconsequencesto hypoxia another small moleculare, i.e., H S, antagonizes ROS
2
plants. effects. In experiments with pea seedlings, treatment with H S
2
significantlyloweredroottipdeathbymitigatingmembranedam-
FLOODING/LOWOXYGEN-INDUCEDPCD agebyROSandsuppressingethyleneproduction.Incontrast,the
Floodingrepresentsaglobalproblemwhichseriouslydiminishes deathofroottipcellswaspromotedafterapplicationofinhibitors
cropyield.Ithasbeenestimatedthatnowadaysmorethan17mil- ofendogenousH Ssynthesis(Chengetal.,2013).
2
lionkm2ofarablelandarepronetofloodingandincertainareas
the risk of flooding may further increase in the future (Shabala INTEGRATIONOFPCDSIGNALSFROMTHEER,
etal.,2014).Themainproblemtoplantsintheseconditionsisthe CHLOROPLASTS,ANDMITOCHONDRIA
significantlyreducedavailabilityofmolecularoxygenwhichcauses Asalreadydescribedinthepreviouschapter,signalsfromdiffer-
hypo-oranoxia.Toalleviatethesymptomsrelatedtohypo/anoxia, ent types of abiotic cues are often generated in specific cellular
plantsresorttoadefensestrategywhichinvolvestheformationof compartmentslikechloroplasts,mitochondria,ortheER.These
specificairchannelsinthesubmergedtissuescalledaerenchyma. organellesarepronetostressbutinthesametimepossessmech-
These interconnected cellular spaces facilitate gas diffusion and anismstoprocesstheinformationinaccordancetotheintensity
reducethemetabolicrequirementsofthefloodedorgans(Leno- ofthestressoraswellasthedevelopmentalstageandtheprevious
chovaetal.,2009).Aerenchymaisformedaftercellsareselectively experienceoftheplant.ThelocalmetabolicimbalancesandROS
eliminated by a PCD process that shares some similarities with accumulationcausedbytheharmfulabioticconditionsproduce
apoptosis and cytoplasmic cell death in animals (Gunawardena signalswhichareintegratedandrelayedtootherpartsofthecell,
etal.,2001). includingthenucleus,andasaresultcellularphysiologyandbio-
Numerous lines of evidence support the notion that ethy- chemistry are readjusted (Suzuki etal.,2012) to allow the plant
lene and ROS are both integral parts of the mechanism of toadapt. However,shouldthedamagecausedbythestressorbe
aerenchyma development. For example, Steffens etal. (2011) insurmountable,aPCDprogrammaybeinduced.
demonstrated that exogenous application of H O stimulates
2 2
lysigenous aerenchyma emergence in rice stems. Moreover, one CHLOROPLASTS,MITOCHONDRIA,ANDTHEIRROLEINPCD
of the highly upregulated genes during waterlogging in maize As the organelles in which photosynthesis occurs, chloroplasts
is Rboh, which, as mentioned earlier, is a major ROS producer areextremelysensitivetoabioticfactors,especiallythoserelated
(Rajhi etal., 2011). In addition, accompanying mitochondrial to light and UV irradiation. Due to the intensive energy fluxes,
dysfunction and the accumulation of metal ions during flood- constantelectrontransport,andthedemandforreducingpower
ingalsoincreaseROSconcentration(Shabalaetal.,2014).Onthe theyareamongthemajorsitesof ROSproductioninplantcells
otherhand,itislongknownthatethylenesynthesisisenhanced (BaierandDietz,2005).Informationofthecurrentredox-status
inalow-oxygenenvironmentandsubsequentlyethylenetriggers of these organelles, which reflects also the ROS concentrations,
PCD (He etal., 1996a,b). In a recent study it was shown that maybetransmittedbymonitoringthestateoftheplastoquinone,
treatmentofwheatseedlingswiththeprecursorofethylene,i.e.,1- ascorbate, and glutathione pools (Foyer and Noctor, 2009).
aminocyclopropanecarboxylicacid(ACC),promotesaerenchyma Chloroplasts,aswellasmitochondria,sendsignalstothenucleus,
formationsimilartoH O buttheadditionof theNADPHoxi- a process known as retrograde signaling (Suzuki etal., 2012),
2 2
dase inhibitor diphenyleneiodonium chloride (DPI) suppresses and in this way they may influence the expression of numerous
the effect of ACC (Yamauchi etal., 2014). Applying DPI alone genesinaccordancewiththeirredoxcondition,includingtriggers
preventsthespreadof submergence-dependentaerenchymafor- ofPCD.
mation(Parlantietal.,2011). Thesefindingssupportthemodel Awell-studiedexampleistheabilityof1O toinitiatesuicide
2
thatROSareessentialforaerenchymadevelopmentandpartici- responses.1O isgeneratedmainlybyexcitedtripletstatechloro-
2
pateinthetransductionofanethylenesignalfromwhichtheyact phyll, photosensitizers like protochlorophyllide in the presence
downstream. A similar mechanism involving ethylene and ROS of light or in the PSII light harvesting complex when the elec-
operatesinepidermalcellswhichneedtoundergoPCDinorder tron transport chain is over-reduced as a result of stress (Apel
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Petrovetal. ROS-mediatedabioticstress-inducedPCD
and Hirt, 2004). To achieve 1O accumulation, scientists have thetransitionporesintheoutermembranethuslettingcytcpass
2
often applied a dark-to-light shift of the conditional flu mutant intothecytosol(Ottetal.,2007).Inplantsthereisnoevidencethat
of Arabidopsis, which retains high levels of the chlorophyll pre- cytccandirectlyactivatePCD(ReapeandMcCabe,2008),butit
cursor and photosensitizer protochlorophyllide (op den Camp appearstobeoneoftheprerequisites,togetherwithROS(Vacca
etal., 2003; Laloi etal., 2007). Work with this mutant has pro- etal.,2006).IthasbeenproposedthatwhenthePTPareopenand
videdevidencethat1O doesnotinducePCDmerelyduetoits cytcisdissipated,evenmoreROSaregeneratedinthemitochon-
2
cytotoxiceffects,butactuallyswitchesonageneticallycontrolled drial electron transport chain (mtETC), which forms a positive
program driven by factors like EXECUTER1 and EXECUTER2 feedbacklooptoamplifytheoriginalsignal(ReapeandMcCabe,
(Leeetal.,2007).Thelight-dependentreleaseof1O alonecannot 2008). Therefore, the cyt c leakage seems to mark the“point of
2
provoke cell death, but needs in addition the blue light-specific no return”after which PCD execution is inevitable. Similarly to
photoreceptor cryptochrome (Danon etal., 2006). Suppressor chloroplasts, mitochondria can also produce retrograde signals
mutants of the flu mutation called singlet oxygen-linked death to notify the nucleus of their current stress status. An example
activators (soldat), in which the 1O -induced cell death is elim- istheTFANAC013inArabidopsis whichwasrecentlydescribed
2
inated,havealsobeenfound(Colletal.,2009;Meskauskieneetal., to convey information about mitochondrial dysfunction to the
2009).A1O -provokedPCDisalsoobservedintheoep16mutant, nucleusandtoleadtoincreasedoxidativestresstolerance.Interest-
2
which is defective in NADPH:protochlorophyllide oxidoreduc- ingly,ANAC013islocatedintheERundernon-stressconditions,
taseAimportandaccumulatesprotochlorophyllide(Samoletal., whichdemonstratesthetightphysicalandfunctionalinteractions
2011).Anotherwayof1O accumulationisobservedinthepre- betweentheERandthemitochondria(DeClercqetal.,2013).
2
viously mentioned chlorina (ch1) mutant, which is deficient in
chlorophyllb(Rameletal.,2013).The1O2-inducedgeneexpres- THEERANDITSROLEINPCD
sioninchlresemblesflu.Moderatelyelevatedlightintensitiescan TheERisanorganellewithessentialfunctionsforproteinsort-
repressthejasmonatepathwayandinduceacclimation,whilejas- ing, post-translational modifications (such as N-glycosylation),
monatesignalingisstronglyinducedbyhighlightintensitiesthat and proper folding (Csala etal., 2006). In case these processes
triggerPCD(Rameletal.,2013). are impaired due to detrimental environmental factors, a spe-
AnotherROSspecies,i.e.,hydrogenperoxide,appearstoantag- cific phenomenon termed as “ER stress” can ensue, which is
onizetheeffectsof 1O inchloroplasts(Laloietal.,2007)which characterized by the accumulation of misfolded proteins (Cai
2
supportstheideathattheidentityoftheROSsignalisofprimary etal.,2014). Adaptation to ER stress is achieved through the so
importancefortheensuingoutcome.Inanotherstudyitwasfound called unfolded protein response (UPR),in the course of which
thatinArabidopsiscellsuspensionculturesonlythetreatmentwith signals from the ER are sent to the nucleus, which in turn
the1O -producingchemicalRoseBengal(RB),butnotwithH O increases the protein folding capacity of the cell (Watanabe and
2 2 2,
triggersPCD,againconfirmingtheimportanceofthenatureofthe Lam, 2009). TFs like CabZIP1 from pepper and AtbZIP28 and
ROSsignal(Gutierrezetal.,2014).Moreover,theseauthorsshow AtbZIP60fromArabidopsis,whichparticipateinthetransduction
that the 1O -mediated cell death program requires functional oftheUPR,arealreadyknowntocontributetoresistancetoabi-
2
chloroplastssincedark-incubatedcells,whichlackthem,hadthe otic stressors like heat, drought, and high salinity (Fujita etal.,
PCD response suppressed. Arabidopsis cell suspension cultures 2007; Gao etal., 2008a; Moreno and Orellana, 2011). However,
were used to investigate also the apoptotic-like PCD (AL-PCD) when the ER stress signal is too intense, a cell death program
◦
thatfollowsaheatshocktreatmentat55 C(Doyleetal.,2010). is triggered instead (Boyce and Yuan, 2006). Recently, the Ara-
However,inthiscasethepresenceofviablechloroplastsseemedto bidopsis membrane-associated TF ANAC089, which relocates to
reducetheoccurrenceofAL-PCDattheexpenseofnecroticcell the nucleus under severe ER stress, was identified as one of
death.Inaddition,treatmentofchloroplast-containingcellswith the controllers that cause PCD in such conditions (Yang etal.,
antioxidantsincreasedtheproportionofAL-PCDanddecreased 2014).
thenumberofnecroticcellswhichdemonstratesthecrucialrole Similartoothervarietiesofstress-inducedPCD,ROStakepart
of plastid-originatedROSforPCDregulation. Apossibleexpla- intheER-PCDaswell,mostlybyprovokingthemobilizationof
nation of these observations could be that cultures containing Ca2+fromtheERtomitochondria,whereCa2+opensthemito-
chloroplasts, which are major ROS producing sites, more easily chondrialPTPs(Williamsetal.,2014).Thisprovesoncemorethat
losecontroloftheirROSmetabolismaftertheheatshock,which the ER and mitochondria can exchange information and inte-
preventsthegeneticallyorganizedPCDprocessandleadstothe gratecommonPCDsignals.AsinothercasesofPCDtriggeredby
morechaoticnecrosisinstead. adverseconditions,theVPEcanbeimplicatedintheexecutionof
Asmentionedearlier, mitochondriaareactiveparticipantsin thecelldeathprogramduringsevereERstress.Insoybean(Glycine
abiotic stress-induced PCD. The decrease of (cid:2)(cid:3)m, most often max), forexample,VPEmaybeswitchedonbythecooperative
accompaniedbythereleaseof cytochromec, arecommonearly action of two NAC TFs, i.e., GmNAC30 and GmNAC81, which
markersofplantPCDastheyareinanimals(Yaoetal.,2004).This togetherintegratebothER-andosmoticstress-inducedcelldeath
inturnresultsintheoxidationof anumberof macromolecules, responses(Mendesetal.,2013).
includinglipids.Theoxidationofcardiolipinnegativelyinfluences AmongthenumerousPCDregulatorsinanimals,muchatten-
thestrengthofcytochromecbindingtotheinnermitochondrial tionhasbeenpaidontheBCL2-associatedXprotein(BAX),asa
membraneandleadstoitsdiffusionintotheintramembranespace. pro-apoptoticfactor,andonBAXinhibitor-1(BI-1),asananti-
Atthesametime,theoxidativestresscausespermeabilizationof apoptotic protein (Isbat etal., 2009). No BAX homologs have
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