ROS Regulation During Abiotic Stress Responses in Crop Plants

15 Pages·2015·0.98 MB·English

by  Zhulong Chan

REVIEW
published:08December2015
doi:10.3389/fpls.2015.01092
ROS Regulation During Abiotic
Stress Responses in Crop Plants
JunYouandZhulongChan*
KeyLaboratoryofPlantGermplasmEnhancementandSpecialtyAgriculture,WuhanBotanicalGarden,ChineseAcademyof
Sciences,Wuhan,China
Abiotic stresses such as drought, cold, salt and heat cause reduction of plant growth
and loss of crop yield worldwide. Reactive oxygen species (ROS) including hydrogen
•− •
peroxide (H O ), superoxide anions (O ), hydroxyl radical (OH ) and singlet oxygen
2 2 2
(1O ) are by-products of physiological metabolisms, and are precisely controlled by
2
enzymatic and non-enzymatic antioxidant defense systems. ROS are significantly
accumulated under abiotic stress conditions, which cause oxidative damage and
eventually resulting in cell death. Recently, ROS have been also recognized as key
playersinthecomplexsignalingnetworkofplantsstressresponses.Theinvolvementof
ROSinsignaltransductionimpliesthattheremustbecoordinatedfunctionofregulation
networkstomaintain ROSat non-toxiclevels in adelicate balancing act between ROS
production,involvingROSgeneratingenzymesandtheunavoidableproductionofROS
during basic cellular metabolism, and ROS-scavenging pathways. Increasing evidence
showed that ROS play crucial roles in abiotic stress responses of crop plants for the
activation of stress-response and defense pathways. More importantly, manipulating
Editedby:
RichardSayre, ROS levels provides an opportunity to enhance stress tolerances of crop plants under
NewMexicoConsortium a variety of unfavorable environmental conditions. This review presents an overview of
atLosAlamosNationalLabs,USA
current knowledge about homeostasis regulation of ROS in crop plants. In particular,
Reviewedby:
wesummarizetheessentialproteinsthatareinvolvedinabioticstresstoleranceofcrop
ThomasLeustek,
Rutgers,TheStateUniversity plantsthroughROSregulation.Finally,thechallengestowardtheimprovementofabiotic
ofNewJersey,USA
stresstolerancethroughROSregulation incropsarediscussed.
VasileiosFotopoulos,
CyprusUniversityofTechnology,
Keywords:cropplants,transcriptionfactors,reactiveoxygenspecies,abioticstress,antioxidativeenzymes,gene
Cyprus regulation
*Correspondence:
ZhulongChan
INTRODUCTION
[email protected].
Abiotic stress conditions such as drought, heat, or salinity affect plant growth and reduce
Specialtysection:
Thisarticlewassubmittedto agricultural production worldwide. These reductions result from climate change and the
PlantPhysiology, freshwater-supply shortage as well as the simultaneous occurrence of different abiotic
asectionofthejournal stresses (Mittler and Blumwald, 2010; Hu and Xiong, 2014). To meet the demands of
FrontiersinPlantScience food security in the face of an increasing world population and environmental challenge,
Received:12August2015 scientists envisage a crucial need for a “second green revolution” to enhance crop
Accepted:20November2015
Published:08December2015 Abbreviations: ABA,abscisicacid;AOX,alternativeoxidases;APX,ascorbateperoxidase;AsA,ascorbicacid;ASR,ABA-,
Citation: stress-,andripening-induced;BR,brassinosteroid;CCaMK,calcium/calmodulin-dependentproteinkinase;CDPK,calcium-
dependentproteinkinase;CIPK,calcineurinB-likeprotein-interactingproteinkinase;DHAR,dehydroascorbatereductase;
YouJandChanZ(2015)ROS
GPX,glutathioneperoxidase;GR,glutathionereductase;GRX,glutaredoxin;GSH,reducedglutathione;GST,glutathione
RegulationDuringAbioticStress S-transferase;MAPK,mitogen-activatedproteinkinase;MAPKKK,MAPKkinasekinase;MDHAR,monodehydroascorbate
ResponsesinCropPlants. reductase;MT,metallothionein;PAs,polyamines;POD,peroxidase;PRX,peroxiredoxin;RBOH,respiratoryburstoxidase
Front.PlantSci.6:1092. homolog;RCD,radical-inducedcelldeath;ROS,reactiveoxygenspecies;SOD,superoxidedismutase;SRO,similartoRCD
doi:10.3389/fpls.2015.01092 one;TRX,thioredoxin.
FrontiersinPlantScience|www.frontiersin.org 1 December2015|Volume6|Article1092
YouandChan ROSRegulationinCropPlants
yieldandyieldstabilityundernon-optimalandadversegrowing Overproduction of ROS caused by stressconditions in plant
conditions byacombination ofapproachesbasedontherecent cells is highly reactive and toxic to proteins, lipids, and nucleic
advancesingenomicresearch(Zhang,2007;Eckardtetal.,2009). acidwhichultimatelyresultsincellulardamageanddeath(Gill
Tocopewithadverseconditions,plantshaveevolvedarange andTuteja,2010).Ontheotherhand,theincreasedproduction
of physiological and metabolic responses by activation of a of ROS during stresses also thought to act as signals for the
great many of stress-responsive genes and synthesis of diverse activation of stress response pathways (Baxter et al., 2014).
functional proteins through a complex signal transduction Plants have evolved an efficient enzymatic and non-enzymatic
network,soastoconfertolerancetotheenvironmentalstresses antioxidative system to protect themselves against oxidative
(HirayamaandShinozaki,2010).Reactiveoxygenspecies(ROS), damage and fine modulation of low levels of ROS for signal
•−
includinghydrogenperoxide(H O ),superoxideradical(O ), transduction.
2 2 2
hydroxyl radical(OH•)and singletoxygen (1O )etc.,resulting ROS-scavenging enzymes of plants include superoxide
2
from excitation or incomplete reduction of molecular oxygen, dismutase (SOD), ascorbate peroxidase (APX), catalase
areharmfulby-products ofbasiccellularmetabolism inaerobic (CAT), glutathione peroxidase (GPX), monodehydroascorbate
organisms (Apel and Hirt, 2004; Miller et al., 2010). Besides reductase (MDHAR), dehydroascorbate reductase (DHAR),
the toxicity of ROS, ROS are also considered to be signaling glutathione reductase (GR), glutathione S-transferase (GST),
molecules that regulate plant development, biotic and abiotic and peroxiredoxin (PRX). These antioxidant enzymes are
stressresponses(ApelandHirt,2004;Mittleretal.,2004).Many located in different sites of plant cells and work together to
excellent reviews have focused on ROS metabolism (Apel and detoxify ROS. SOD acts as the first line of defense converting
•−
Hirt, 2004; Noctor et al., 2014), ROS sensory and signaling O into H O . CAT, APX, and GPX then detoxify H O . In
2 2 2 2 2
networks (Miller et al., 2010; Suzuki et al., 2012; Baxter et al., contrast to CAT, APX requires an ascorbic acid (AsA) and/or
2014), as well as the cross-talk with other signaling molecules a glutathione (GSH) regenerating cycle involved MDHAR,
functionindevelopmentalandstressresponseprocesses(Suzuki DHAR,andGR.GPX,GST,andPRXreduceH O andorganic
2 2
etal.,2012;Noctoretal.,2014).However,mostofthesereviews hydroperoxides through ascorbate-independent thiol-mediated
provided an overall retrospective for model plant Arabidopsis. pathways using GSH, thioredoxin (TRX) or glutaredoxin
Gill and Tuteja (2010) reviewed enzymatic and non-enzymatic (GRX) as nucleophile (Dietz et al., 2006; Meyer et al., 2012;
antioxidants and their roles in abiotic stress tolerance of crop Noctor et al., 2014). Non-enzymatic antioxidants include
plants. However, the regulation mechanism of the antioxidant GSH, AsA, carotenoids, tocopherols, and flavonoids are also
system and the key components involved in ROS regulation crucial for ROS homeostasis in plant (Gill and Tuteja, 2010).
and abiotic stress tolerance have not yet been summarized in Besides traditional enzymatic and non-enzymatic antioxidants,
crop plants. In this review, we provide an overview of current increasing evidences indicated that soluble sugars, including
knowledge about ROS homeostasis regulation in crop plants. disaccharides, raffinose family oligosaccharides and fructans,
In particular, the genes that have been characterized in ROS have a dual role with respect to ROS (Couee et al., 2006;
homeostasisregulationaffectingabioticstressresistanceincrop Keunen et al., 2013). Soluble sugars were directly linked with
plantsweresummarized. the production rates of ROS by regulation ROS producing
metabolic pathways, such as mitochondrial respiration or
photosynthesis. Conversely, they also feed NADPH-producing
ROS HOMEOSTASIS IN PLANT metabolism to participate in antioxidative processes (Couee
etal.,2006).
Theevolutionofaerobicmetabolicprocessessuchasrespiration In addition to the antioxidative system, avoiding ROS
and photosynthesis unavoidably led to the production of ROS production by alleviating the effects of stresses on plant
in mitochondria, chloroplast, and peroxisome (Apel and Hirt, metabolismmayalsobeimportantforkeepingROShomeostasis.
2004;GillandTuteja,2010).Underoptimalgrowth conditions, Alternativeoxidases(AOX)canpreventtheexcessgenerationof
intracellularROSaremainlyproducedatalowlevelinorganelles. ROSinthe electrontransport chainsofmitochondria (Maxwell
However,ROSaredramaticallyacclimatedduringstress.Under et al., 1999). By diverting electrons flowing through electron-
abiotic stress condition, limitation of CO uptake, caused transport chains, AOX can decrease the possibility of electron
2
•−
by stress-induced stomatal closure, favors photorespiratory leakingtoO togenerateO .Othermechanisms,suchasleaf
2 2
production of H O in the peroxisome and production of movement and curling, photosynthetic apparatus rearranging,
2 2
superoxide and H O or singlet oxygen by the overreduced mayalsorepresentanattempttoavoidtheover-reductionofROS
2 2
photosynthetic electron transport chain (Apel and Hirt, 2004; bybalancingtheamountofenergyabsorbedbytheplantwiththe
Noctoretal.,2014).Inadditiontoorganelles,plasmamembrane availabilityofCO (Mittler,2002).
2
together with apoplast is the main site for ROS generation in
response to endogenous signals and exogenous environmental
REGULATION OF NADPH OXIDASES IN
stimuli. Several types of enzymes, such as NADPH oxidases,
amineoxidases,polyamineoxidases,oxalateoxidases,andalarge CROP PLANTS
family of class III peroxidases, that localized at the cell surface
orapoplastarecontributedtoproductionofapoplastROS(Apel PlantNADPHoxidases,alsoknownasrespiratoryburstoxidase
andHirt,2004;CosioandDunand,2009;GillandTuteja,2010). homologs (RBOHs), are the most studied enzymatic source
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YouandChan ROSRegulationinCropPlants
of ROS. Plant RBOHs have cytosolic FAD- and NADPH- during pathogen defense (Kobayashi et al., 2007). In tobacco,
bindingdomainsintheC-terminalregion,andtransmembrane NbRBOHA and NbRBOHB are in charge of the generation of
domains that correspond to those in mammalian NADPH ROSduringthedefenseresponse(Yoshiokaetal.,2003).Further
oxidases (Suzuki et al., 2011). In addition, plant RBOHs have study indicated that mitogen-activated protein kinase (MAPK)
a cytosolic N-terminal extension contains regulatory regions cascades MEK2-SIPK/NTF4 and MEK1-NTF6 were involved
such as calcium-binding EF-hands and phosphorylation target in the NbRBOHB-dependent oxidative burst in response to
sites that are important for the function and regulation of pathogen signals (Asai et al., 2008). Two tomato RBOH genes,
the plant NADPH oxidases (Oda et al., 2010; Suzuki et al., SlRBOHB (SlWfi1) and SlRBOHG (SlRBOH1), have turned out
2011). Increasing evidence demonstrated NADPH oxidases to participate in wounding response and development (Sagi
as key signaling nodes in the ROS regulation network of et al., 2004). Other studies revealed that SlRBOHG (SlRBOH1)
plants integrating numerous signal transduction pathways with isvitalforbrassinosteroid(BR)-inducedH O production,ABA
2 2
ROS signaling and mediating multiple important biological accumulation, stomatal closure/opening and oxidative stress
processes,including cellgrowth andplantdevelopment,abiotic tolerance (Xia et al., 2014; Zhou et al., 2014a), while SlRBOHB
stress response and adaptation, plant–microbe pathogenic was found to positively regulate the defense response against
and symbiotic interactions (Torres and Dangl, 2005; Suzuki B. cinerea, the flg22-induced immune response and drought
et al., 2011; Marino et al., 2012). Numerous studies have stress response (Li et al., 2015). Lin et al. (2009) observed
uncovered several regulatory mechanisms of plant NADPH that the activity of NADPH oxidase is regulated by H O and
2 2
oxidases in Arabidopsis, which involved various signaling ZmMPK5 in maize. Zhu et al. (2013b) identified a BR induced
components including protein phosphorylation, Ca2+, microtubule-associated protein, ZmMAP65-1a,interacts with a
CDPKs, and phospholipase Dα1 (PLDα1) (Baxter et al., MAPK and functions in H O self-propagation by regulating
2 2
2014). Ca2+ regulates NADPH oxidase-dependent ROS the expression of NADPH oxidase genes in BR signaling in
production by binding directly to the EF-hand motif in the N maize.
terminus of RBOH protein and/or regulating Ca2+-dependent
phosphorylation medicated by CDPK (Ogasawara et al.,
REGULATION OF ANTIOXIDATIVE
2008; Dubiella et al., 2013). RBOHs were also found to be
phosphorylated by SnRK2 protein kinase OPEN STOMATA 1 SYSTEM IN CROP PLANTS
(OST1) during ABA-dependent stomatal closure (Sirichandra
etal.,2009). Plantantioxidative system consists ofnumerous enzymatic and
Functions and regulatory mechanisms of several RBOH non-enzymatic antioxidative components that work together
proteins were investigated in crops. The activity of NADPH with ROS-generating pathway to maintain ROS homeostasis.
oxidase was increased by drought, and exhibited high- Several studies showed important roles of antioxidative
temperature stability and an alkaline-philic feature, suggesting components in ROS homeostasis in crop plants. The rice
its important role in response to drought stress (Duan et al., (japonica) genome has eight genes that encode putative SODs,
2009). Treatment with ABA and Ca2+ also considerably including two cytosolic copper-zinc SODs (cCuZn-SOD1 and
induced the activity of NADPH oxidase in leaves of maize cCuZn-SOD2), one putative CuZn-SOD-like (CuZn-SOD-L),
seedlings(JiangandZhang,2002a,2003).NineNADPHoxidase one plastidic SOD (pCuZn-SOD), two iron SODs (Fe-SOD2
(RBOH) genes (OsRBOHA–OsRBOHI) were identified in the and Fe-SOD3), and one manganese SOD (Mn-SOD1) (Nath
rice genome (Wong et al., 2007). Rice RBOH genes exhibited et al., 2014). Transgenic rice plants overexpressing Mn-SOD1
•−
unique patterns of expression changes in response to various showed less mitochondrial O under stress and reduced the
2
environmental stresses (Wang et al., 2013). A small GTPase stress induction of OsAOX1a/b specifically (Li et al., 2013).
Rac in rice (OsRac1) was identified as a positive regulator of ThereareeightAPXgenesinrice,includingtwocytosolicAPXs
OsRBOHB involved in pathogen defense (Wong et al., 2007). (OsAPX1 and OsAPX2), two peroxisomal APXs (OsAPX3 and
A direct interaction between OsRac1 and the N-terminal OsAPX4),twomitochondrialAPXs(OsAPX5andOsAPX6)and
extension of OsRBOHB may be required for NADPH oxidase twochloroplastic APXs(OsAPX7 and OsAPX8)(Teixeira etal.,
activitymodulatedbythecytosolicCa2+concentrationinplants 2004, 2006). Two cytosolic APXs, OsAPX1 and OsAPX2, have
(Wongetal.,2007).Furthermutationanalysesoftheregulatory crucialrolesinabiotic stressresistance inrice(Satoetal.,2011;
domains of OsRBOHB indicated that not only the EF-hand Zhang et al., 2013). Interestingly, rice mutants double silenced
motif but also the upstream N-terminal region was essentialto for cytosolic APXs (APX1/2s) exhibit significant changes in
Ca2+-dependentbutnot phosphorylation-dependent activation the redox status indicated by higher H O levelsand increased
2 2
(Takahashi et al., 2012). In addition, Liu et al. (2012) found glutathione and ascorbate redox states, triggering alterations in
that phosphatidylinositol 3-kinase (PI3K) regulated NADPH theROSsignalingnetworksandmakingthemutantsabletocope
oxidaseactivitybymodulatingtherecruitmentofRac1toplasma withabioticstresssimilartonon-transformed plants(Bonifacio
membrane. Rice histidine kinase OsHK3 showed to regulate etal.,2011).SomeoftheROS-scavengingenzymes,suchasGST
the expression of NADPH oxidase genes and the production (DixonandEdwards,2010),TRX,andGRX(Meyeretal.,2012),
of H O in ABA signaling (Wen et al., 2015). In potato, two haveevolvedintolargemultigenefamilieswithvariedfunctions
2 2
CDPKs, StCDPK4 and StCDPK5, were found to induce the that cope with a variety of adverse environmental conditions.
phosphorylation ofStRBOHBandregulatedtheoxidative burst Recent mutational and transgenetic plants analyses revealed
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YouandChan ROSRegulationinCropPlants
special member of multigene enzyme family as a key player in is also necessary for ABA-induced antioxidant defense (Zhang
ROS homeostasis regulation in crop plants. OsTRXh1, encodes et al., 2014). Moreover, ABA-induced H O production and
2 2
h-type TRX in rice, regulates the redox state of the apoplast ABA-inducedactivation of OsMPKspromote the expression of
and participates in plant development and stress responses ZFP36,and ZFP36 also up-regulates the expression of NADPH
(Zhang et al., 2011). OsTRXh1 protein possesses reduction oxidase and MAPK genes and the production of H O in
2 2
activityandsecretedintotheextracellularspace.Overexpression ABA signaling (Zhang et al., 2014). In maize, ABA and H O
2 2
of OsTRXh1 produce less H O under salt stress, reduce the increased the expressionandthe activity ofZmMPK5,whichis
2 2
expression of the salt-responsive genes, lead to a salt-sensitive required for ABA-induced antioxidant defense. The activation
phenotype in rice. In another study, Perez-Ruiz et al. (2006) of ZmMPK5 also enhances the H O production by increasing
2 2
reported that rice NADPH thioredoxin reductase (NTRC) the expression and the activity of NADPH oxidase, thus there
utilizes NADPH to reduce the chloroplast 2-Cys PRX BAS1, is a positive feedback loop involving NADPH oxidase, H O ,
2 2
thus protects chloroplast against oxidative damage by reducing and ZmMPK5 in ABA signaling (Zhang et al., 2006; Hu et al.,
H O . 2007;Dingetal.,2009;Linetal.,2009).Subsequentexperiments
2 2
The involvement of ROS in signal transduction implies that confirmed that ABA-induced H O production mediates NO
2 2
there must be coordinated function of regulation networks to generation in maize leaves, which, in turn, activates MAPK
maintain ROS at non-toxic levels in a delicate balancing act and increases the expression and the activities of antioxidant
betweenROSproductionandROS-scavengingpathways,andto enzymes in ABA signaling (Zhang et al., 2007). Moreover, a
regulate ROS responses and subsequent downstream processes maize CDPK gene, ZmCPK11, acts upstream of ZmMPK5, is
(Mittler et al., 2004). Numerous studies from different plant essential for ABA-induced up-regulation of the expression and
species observed that the generation of ROS and activity of activities of SOD and APX, and the production of H O in
2 2
various antioxidant enzymes increased during abiotic stresses maize leaves (Ding et al., 2013). Hu et al. (2007) found that
(Damanik et al., 2010; Selote and Khanna-Chopra, 2010; Ca2+-CaMisrequiredforABA-inducedantioxidantdefenseand
Tang et al., 2010; Turan and Ekmekci, 2011). There is an functions both upstream and downstream of H O production
2 2
increasing body of literature concerning the mechanisms by in leaves of maize plants. Afterward, Ca2+/CaM-dependent
which regulation of antioxidative system response to abiotic proteinkinase,ZmCCaMK,wasreportedtobeessentialforABA-
stressesin crops. Intrinsic to this regulation is ROS production inducedantioxidantdefense,andH O -inducedNOproduction
2 2
and signaling that integrated with the action of hormone and isinvolvedintheactivationofZmCCaMKinABAsignaling(Ma
smallmolecules. etal.,2012).
The plant hormone ABA is the key regulator of abiotic Brassinosteroids are a group of steroid hormones and
stressresistance inplants,andregulateslargenumberofstress- importantforabroadspectrumofplantgrowthanddevelopment
responsive genes by a complex regulatory network so as to processes, as well as responses to biotic and abiotic stresses
confer tolerance to the environmental stresses (Cutler et al., (Bajguz and Hayat, 2009; Divi and Krishna, 2009; Yang et al.,
2010; Raghavendra et al., 2010). ABA-induced stress tolerance 2011; Zhu et al., 2013a). Numerous studies have shown that
is partly linked with the activation of antioxidant defense BR can activate antioxidant defense systems to improve stress
systems, including enzymatic and non-enzymatic constituents, tolerance in crops (Özdemir et al., 2004; Xia et al., 2009).
which protects plant cells against oxidative damage (Huang Zhang et al. (2010) reported that ZmMPK5 is required for
et al., 2012; Zhang et al., 2012a, 2014). Water stress-induced NADPH oxidase-dependent self-propagation of ROS in BR-
ABA accumulation and exogenous ABA treatment triggers the induced antioxidant defense systems in maize. Further study
increased generation of ROS, then leads to the activation of foundedthata65kDamicrotubule-associatedprotein(MAP65),
the antioxidant system in crops (Jiang and Zhang, 2002a,b; ZmMAP65-1a,directlyphosphorylatedbyZmMPK5,isrequired
Ye et al., 2011). Small molecules, such as Ca2+, calmodulin forBR-inducedantioxidantdefense(Zhuetal.,2013b).Recently,
(CaM),NOandROShavebeendemonstratedtoplayvitalroles Ca2+ and maize CCaMK gene, ZmCCaMK, was demonstrated
in ABA-induced antioxidant defense (Jiang and Zhang, 2003; to be required for BR-induced antioxidant defense (Yan et al.,
Huetal.,2007).Inrice,aCa2+/CaM-dependentproteinkinase 2015).
(CCaMK), OsDMI3, is necessary for ABA-induced increases
in the expression and the activities of SOD and CAT. ABA-
GENES INVOLVED IN ROS REGULATION
inducedH O productionactivatesOsDMI3,andtheactivation
2 2
AND ABIOTIC STRESS TOLERANCE IN
of OsDMI3 also enhances H O production by increasing the
2 2
expression of NADPH oxidase genes (Shi et al., 2012). Further CROPS
studyindicatedthatOsDMI3functionsupstreamofOsMPK1,to
regulatetheactivitiesofantioxidantenzymesandtheproduction To cope with abiotic stress, plants have evolved multiple
ofH O inrice(Shietal.,2014).Recentstudyprovidesevidence and interconnected signaling pathways to regulate different
2 2
to show that rice histidine kinase OsHK3 functions upstream sets of stress-responsive genes for producing various classes
of OsDMI3 and OsMPK1, and is necessary for ABA-induced of proteins, such as protein kinases, transcriptional factors,
antioxidant defense (Wen et al., 2015). Zhang et al. (2012a) enzymes, molecular chaperones, and other functional proteins,
reported that C2H2-type ZFP, ZFP182, is involved in ABA- resultingindiversephysiologicalandmetabolicresponsesoasto
induced antioxidant defense. Another C2H2-type ZFP, ZFP36, confertolerancetotheenvironmentalstresses.Hundredsoreven
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YouandChan ROSRegulationinCropPlants
1000sofgenesthatregulatestressresponseshavebeenidentified tolerance tosalt and drought stresses.GhMKK5-overexpressing
in crop plants by diverse functional genomics approaches (Hu plants showed significantly up-regulated expression of ROS-
andXiong,2014).Inparalleltothis,thefunctions ofnumerous related and cell death marker genes, and resulted in excessive
stress-responsivegenesinvolvedinROShomeostasisregulation accumulation of H O and hypersensitive response (HR)-like
2 2
andabioticstressresistancehavebeencharacterizedintransgenic cell death (Zhang et al., 2012b). In another study, a drought-
plants(Figure1;Table1). hypersensitivemutant(drought-hypersensitivemutant1[dsm1])
ofaputativeMAPKkinasekinasegenehasbeenidentifiedinrice
Protein Kinases and Phosphatases (Ningetal.,2010). The dsm1 mutant wassensitive tooxidative
Mitogen-activated protein kinase cascades are involved in stresswithdown-regulatedexpressionoftwoperoxidase(POD)
diverse processes from plant growth and developmentto stress genesandreducedPODactivity.
responses. MAPK cascades also play crucial roles in ROS Calcium-dependent protein kinase proteins regulate the
signaling, and several studies in Arabidopsis have shown that downstream components in calcium signaling pathways.
ROS are not only the trigger, but also the consequence of A rice CDPK gene, OsCPK12, enhances tolerance to salt stress
activation of MAPK signaling (Kovtun et al., 2000; Pitzschke by reducing the accumulation of ROS (Asano et al., 2012).
and Hirt, 2006; Pitzschke et al., 2009). However, few MAPK Expression of genes encoding ROS-scavenging enzymes
cascades components have been functionally characterized in (OsAPx2 and OsAPx8) were up-regulated, whereas the
crops.TwoMAPKkinases(MAPKKs),GhMKK1andGhMKK5 NADPH oxidase gene (OsRBOHI) was down-regulated in
have been characterized to be involved in stress resistance and OsCPK12-overexpressingplantscomparedwithwildtypeplants.
ROS homeostasis in cotton (Zhang et al., 2012b; Lu et al., Conversely, the oscpk12 mutant and RNAi plants were more
2013). Overexpression of GhMKK1 in tobacco improved its sensitive to high salinity and accumulated more H2O2 than
tolerance to salt and drought stresses, exhibited an enhanced wildtypeplants(Asanoetal.,2012).Overexpressionofanother
ROSscavengingcapabilityandsignificantlyelevatedactivitiesof CDPK gene, OsCPK4, results in increased tolerance to salt and
antioxidantenzymes(Luetal.,2013).Whereas,overexpressionof droughtstressesinriceplants.Transgenicplantsexhibitedhigher
anothercottonMAPKKgene,GhMKK5,intobaccoreducedtheir expressionofnumerousgenesinvolvedinlipidmetabolismand
FIGURE1|OverviewofmajorgenesthatinvolvedinabioticstressresistancethroughROSregulationincropplants.Plantcellsperceiveabioticstress
signalsandtransducethemthroughvarioussignalingpathwaysincludingsecondarysignalingmolecules,planthormones,andtranscriptionalregulators.The
regulationofgeneexpressionbydifferenttranscriptionregulatorsresultsintheinductionofvariousdefensepathways,suchas,reactiveoxygenspecies(ROS)
scavengingandantioxidativemetabolism.TranscriptionregulatorsalsomediateROSproducingsystemsandactivatetheexpressionofstress-responsivegeneso
astoconfertolerancetotheenvironmentalstresses.CDPK,calcium-dependentproteinkinase;CIPK,calcineurinB-likeprotein-interactingproteinkinase;MAPK,
mitogen-activatedproteinkinase;PK,proteinkinase;PP,proteinphosphatase;SRO,similartoRCDone.
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YouandChan ROSRegulationinCropPlants
Reference Luetal.,2013 Ningetal.,2010 Campoetal.,2014 Asanoetal.,2012 Dengetal.,2013 Huetal.,2015 Lietal.,2014 Youetal.,2014 Huangetal.,2009 Zhangetal.,2014 Janetal.,2013 Schmidtetal.,2013 Fukaoetal.,2011 Wuetal.,2008 Wangetal.,2015 Yanetal.,2014 Wangetal.,2015 Fangetal.,2015 Huetal.,2013 Youetal.,2013 Liuetal.,2014 Houetal.,2009 Duetal.,2010 Zhangetal.,2009 McKersieetal.,1996 Zhangetal.,2013 (Continued)
s
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d d
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on. ROSregulation ROSscavenging ROSscavenging ROSscavenging ROSproductionascavenging ROSscavenging ROSscavenging;antioxidativemetabolism ROSproduction ROSscavenging ROSscavenging ABA-inducedantioxidantdefens ROSscavenging ROSsignaling ROSscavenging ROSscavenging ROSproduction ROSscavenging ROSproduction ROSscavenging ROSscavenging ROSscavenging ROSproductionascavenging ROSscavenging antioxidativemetabolism ABA-inducedantioxidantdefens ROSscavenging ROSscavenging
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hroughROSreg Transformationreceptor N.benthamiana O.sativa O.sativa O.sativa N.benthamiana Malusxdomestica;S.lycopersicum O.sativa O.sativa O.sativa O.sativa O.sativa O.sativa O.sativa N.benthamiana G.max N.benthamiana G.max O.sativa N.benthamiana O.sativa T.aestivum;A.thaliana O.sativa O.sativa N.benthamiana M.sativa O.sativa
t
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anceinmajorcro Origin G.hirsutum O.sativa O.sativa O.sativa T.aestivum Malusxdomestica O.sativa O.sativa O.sativa O.sativa O.sativa O.sativa O.sativa S.lycopersicum G.max G.hirsutum G.max O.sativa T.aestivum O.sativa T.aestivum O.sativa O.sativa S.guianensis N.plumbaginifolia O.sativa
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vedinabioticstressre Proteinfunction MAPKK MAPKKK calcium-dependentproteinkinase calcium-dependentproteinkinase CBL-interactingproteinkinase CBL-interactingproteinkinase Lectinreceptor-likekinase Proteinphosphatase2C C2H2zincfinger C2H2zincfinger CCCHzincfinger ERF ERF ERF WRKY WRKY NAC NAC ASR SRO SRO Ski-interactionprotein Carotenehydroxylase 9-cis-epoxycarotenoid MnSOD APX
ol
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genesthatin Genes GhMKK1 DSM1 OsCPK4 OsCPK12 TaCIPK29 MdSOS2L1 SIT1 OsPP18 DST ZFP36 OsTZF1 SERF1 SUB1A JERF3 GmWRKY27 GhWRKY17 GmNAC29 SNAC3 TaASR1 OsSRO1c Ta-sro1 OsSKIPa DSM2 SgNCED1 MnSOD OsAPX2
e
v
TABLE1|Representati Functionalcategory Proteinkinase MAPKs CDPK CIPK Otherkinase Proteinphosphatase Transcriptionfactors Zincfinger AP2/ERF WRKY NAC OtherTF Othernuclearproteins SROprotein Other ABAmetabolism ROSscavenging
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YouandChan ROSRegulationinCropPlants
0 protection against oxidative stress, therefore, reduced levels of
0
0
Reference Oberschalletal.,2 Yangetal.,2009 Xueetal.,2009 Hudaetal.,2013 Wangetal.,2011 Youetal.,2012 Tutejaetal.,2013 Dongetal.,2013 mefOotvueaCemnl.r,daeb2lxrc0ptaiou1nr4emesb)s.-elidiopernipedsepnopofdenreownsixthvieedpaartttooitoCenaiInbPuiKokntidincegaressnetsreteprserTssoastvCeciiIaonPnsKRda2Oilt9siSoonirnhseag(vtuCoelbaabtmaiecopecnono.
resultedinincreasedsalttolerance.Transgenictobaccoseedlings
maintained high K+/Na+ ratios and Ca2+ content by up-
es regulating the expression of some transporter genes, and also
stressresistance andoxidativestress stress saltandcoldstress andsaltstress stress andoxidativestress andsaltstress oxidativestress raeaeettpcdtpaaiuvllle..ci,,,tei22dea00sl1s1Ro5o3O)f).c.SRoMOnOavofcSeelcer-rurscemecuxdapluavrrleseanasatlsigntoiioanntnlogsylseobiersfynaazMniynncmddecSrefOeiusnaSnsu2iacnnLtpigd1po,elnterahalesaCancelIhdtPxapKsrttraorecgmestesseasniroteio(znDafrt(aeoiHonnmnudg
Abiotic Drought Drought Drought, Drought Drought Drought Drought Saltand oenfzMymdSesOaSn2Ld1anextihoixbiidteadntthmaettaitboinlictreesasseuschthaesRpOroScysacnaivdeinngianngd-
malate,leading to enhanced salt tolerance in apple and tomato
(Huetal.,2015).Aricelectinreceptor-likekinase,saltintolerance
1(SIT1)wasdemonstratedmediatessaltsensitivitybyregulating
e ROSandethylenehomeostasisandsignaling(Lietal.,2014).SIT1
s
ROSregulation antioxidativemetabolism ROSscavenging ROSscavenging ROSscavenging ROSscavenging antioxidativemetabolism;ROSscavenging ROSscavenging ABA-inducedantioxidantdefen pSusiIhngTodnT1seah.prlSiehnsIoagTdrl-e1tydplpseahtprtroeoeessmnspsMdho,eotPwnerKsthylam3iaccthaacinonuodnmnce6cumr,ul(aareLtnrdieidoidaentttheioandelfi.,Rrab2nOay0cS1Mtpi,4vrl)Poea.tKateido3iinn/n6gbp-ythaoosnapsdplltahenratethtqadyuseleiearnteihess
an important event in the signal transduction process that
regulates various cellular activities. A rice protein phosphatase
ansformationceptor benthamiana sativa benthamiana benthamiana benthamiana;esculentum sativa sativa aestivum;thaliana d2soeCfonws(RinPtOsiPvtSr2ee-Csatoc)magdvgeerenonneuge,ginO(hYgtsoPauePnn1dez8tyo,amxlw.i,eda2ssa0.t1iidv4Tee)hn.seTttirhfieAeesdsBosAwaps-piti1nha8dSrmueNcdueAutdCacen1det-xerapexcgrhteuiivsblsaiitittioeeendds
Trre N. O. N. N. N.L. O. O. T.A. of ABA-responsive genes has not been disrupted in ospp18
mutant, indicating OsPP18 mediates drought stress resistance
m m by regulating ROS homeostasis through ABA-independent
Origin M.sativa O.sativa G.hirsutu O.sativa P.trifoliata O.sativa O.sativa T.aestivu Tpartahwnasycs(rYipoutieotnal.a,2l0f1a4c).tors
Transcriptionalfactors(TFs)areoneoftheimportantregulatory
Proteinfunction NADPH-dependentaldose/aldehydereductase type1metallothionein Type3metallothionein+2typeIIBCaATPase Argininedecarboxylase Ornithineδ-aminotransferase NTP-dependentRNA/DNAhelicase 12-oxo-phytodienoicacidreductases prasifNnaiolrmtAcloepetCtruoslearlitn()ntdaN,htsnoseAze.wiinoMMnnevucxsoe,stpllmrAfiyvreeenTbaadsgAmesneriiFdsorn,,nooaeafWfnnboAdhisRoftaPCtrKni2eacUYcs/esE,sCstRurbt)soeFZbifgslaseIs(nemPrAartaelPini(lsoniEbcpefegaTossAnthiscocstLaarevAesseleces.n2sauTbv/-dceriehieretenehossny,epnylomcpwezhnlniheapasenyiirpcvatreehaeecrslts)sep,cgesrootneiraznnuteneiselsadddessl
with roles in the regulation of plant abiotic stress responses
Genes MsALR OsMT1a GhMT3a OsACA6 PtADC OsOAT OsSUV3 TaOPR1 tC(hYieaftmmcia-hgYauivlcmehbai-ezSehanninddoemzMaokitnitslaetrnra,dt2e0Sd0ht8ion;boFezaaninkgiv,eot2lv0ae0ld.6,;i2n0AR0r8Oie),Slahentodmalse.o,om2st0ea0so7isf;
regulationandabioticstressresistanceincrops.
Proteins containing zinc finger domain(s) were widely
TABLE1|Continued Functionalcategory Detoxificationproteins Calciumtransporters Polyaminesmetabolism Aminoacidmetabolism Helicase Unknownfunction eiZrdtnhexeApepfTeAoeen1rrtxtisA0mepedPraeegnXnsetds1otnisoZeksbnsAhneoTioonwc1fkk2eesAo,ydoruimtastphbeilainapdtzyltoateiehnpnnrecsstsissesefiilny(nzaMinguntediphclrl-eefirogrenterghgneeuegeetrlrusaalptsialenrp.td,oieoAtc2beni0riyena0sobos8.ifx)wdF.iodRoeSprarOuestiibeSisvnxs-,ereavZeqmsolAtualrpvTeteeelns7eddst,,
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YouandChan ROSRegulationinCropPlants
in ROS regulation and multiple abiotic stresses tolerance SERF1 is essential for the propagation of the initial ROS signal
(Davletova et al., 2005; Mittler et al., 2006; Ciftci-Yilmaz et al., to mediate salt tolerance. SUB1A, an ERF transcription factor
2007). The zinc finger proteins are divided into several types, foundinlimitedriceaccessions,limitsethyleneproduction and
such as C2H2, C2C2, C2HC, CCCH and C3HC4, based on gibberellin responsiveness during submergence, economizing
the number and the location of characteristic residues (Ciftci- carbohydrate reserves and significantly prolonging endurance
YilmazandMittler,2008).Thesignalingpathwaysparticipating (FukaoandXiong,2013).Afterfloodwaterssubside,submerged
in stomatal movement were well studied in the model plant plants encounter re-exposure to atmospheric oxygen, leading
Arabidopsis, but were largely unknown in crops. Huang et al. to postanoxic injury and severe leaf desiccation (Setter et al.,
(2009)identifiedadroughtandsalttolerance (dst) mutant,and 2010; Fukao and Xiong, 2013). SUB1A also positively affects
the DST was cloned by the map-based cloning. DST encoded postsubmergence responses byrestrained accumulation of ROS
a C2H2-type zinc finger transcription factor that negatively in aerial tissue during desubmergence (Fukao et al., 2011).
regulated stomatal closure by direct regulation of genes related Consistently,SUB1ApromptestheexpressionofROSscavenging
toH O homeostasis,whichidentifiedanovelsignalingpathway enzyme genes, resulting in enhanced tolerance to oxidative
2 2
ofDST-mediatedH O -inducedstomatalclosure(Huangetal., stress. On the other hand, SUB1A improves survival of rapid
2 2
2009).LossofDSTfunctionincreasedtheaccumulationofH O dehydration following desubmergence and water deficit during
2 2
inguardcell,accordingly,resultedinincreasedstomatalclosure drought by increasing ABA responses, and activating stress-
and enhanced drought and salt tolerance in rice. Other two inducible gene expression (Fukao et al., 2011). A jasmonate
C2H2-type zinc finger proteins, ZFP36 and ZFP179, also play and ethylene-responsive ERF gene, JERF3, was isolated from
circle role in ROS homeostasis regulation and abiotic stress tomato and involved in a ROS-mediated regulatory module in
resistance in rice. ZFP179 encodes a salt-responsive zinc finger transcriptional networks that govern plant response to stress
proteinwithtwoC2H2-typezincfingermotifs(Sunetal.,2010). (Wu et al., 2008). JERF3 modulates the expression of genes
The ZFP179 transgenic rice plants increased ROS-scavenging involvedinosmoticandoxidativestressesresponsesbybinding
abilityandexpressionlevelsofstress-relatedgenes,andexhibited totheosmotic-andoxidative-responsiverelatedciselements.The
significantlyenhancedtolerancetosaltandoxidativestress(Sun expressionofthesegenesleadstoreduceaccumulationofROS,
etal.,2010).ZFP36isanABAandH O -responsiveC2H2-type resulting in enhanced abiotic stress tolerance in tobacco (Wu
2 2
zinc finger protein gene, and plays a important role in ABA- etal.,2008).
inducedantioxidantdefenseandthetoleranceofricetodrought The WRKY family proteins have one or two conserved
and oxidative stresses (Zhang et al., 2014). Moreover, ZFP36 WRKY domains comprising a highly conserved WRKYGQK
is a major player in the regulation of the cross-talk involving heptapeptide at the N-terminus and a zinc-finger-like motif
NADPH oxidase, H O , and MAPK in ABA signaling (Zhang at the C-terminus (Eulgem et al., 2000). The conserved
2 2
etal.,2014).OsTZF1,aCCCH-tandemzincfingerprotein, was WRKY domain plays important roles in various physiological
identifiedasanegativeregulatorofleafsenescenceinriceunder processes by binding to the W-box in the promoter regions
stressconditions (Janetal.,2013).Meanwhile,OsTZF1 confers of target genes (Ulker and Somssich, 2004; Rushton et al.,
tolerancetooxidativestressinricebyenhancingtheexpressionof 2010). Wang et al. (2015) reported a multiple stress-responsive
redoxhomeostasisgenesandROS-scavengingenzymes(Janetal., WRKY gene, GmWRKY27, reduces ROS level and enhances
2013). A cotton CCCH-type tandem zinc finger gene,GhTZF1, salt and drought tolerance in transgenic soybean hairy roots.
alsoservesasakeyplayerinmodulatingdroughtstressresistance GmWRKY27 interacts with GmMYB174, which, in turn, acts
and subsequent leaf senescence by mediating ROS homeostasis in concert to reduce promoter activity and gene expression of
(Zhouetal.,2014b). GmNAC29 (Wang et al., 2015). Further experiments showed
MembersofAP2/ERF(APETALA2/ethyleneresponsefactor) that GmNAC29 is a negative factor of stress tolerance
transcription factor family, including DREB/CBF transcription for enhancing the ROS production under abiotic stress by
factors, areespeciallyimportant astheyregulategenesinvolved directly activating the expression of the gene encoding ROS
in multiple abiotic stress responses (Mizoi et al., 2012). During production enzyme.In another study, overexpression of cotton
theinitialphaseofabioticstresses,elevatedROSlevelsmightact WRKY gene, GhWRKY17, reduced transgenic tobacco plants
asavitalacclimationsignal.Butthekeyregulatorycomponents tolerance to drought and salt stress. Subsequent experiments
of ROS-mediated abiotic stress response signaling are largely showed that GhWRKY17 involved in stress responses by
unknown. Rice salt- and H O -responsive ERF transcription regulating ABA signaling and cellular levels of ROS (Yan
2 2
factor, SERF1, has a critical role in regulating H O -mediated et al., 2014). Sun et al. (2015) isolated a WRKY gene,
2 2
molecularsignalingcascadeduringtheinitialresponsetosalinity BdWRKY36, from B. distachyon, and found it functions as a
inrice (Schmidtetal.,2013).SERF1regulatestheexpressionof positive regulator of drought stress response by controlling
H O -responsivegenesinvolvedinsaltstressresponsesinroots. ROS homeostasis and regulating transcription of stress-related
2 2
SERF1isalsoaphosphorylationtargetofasalt-responsiveMAPK genes.
(MAPK5), and activation the expression of salt-responsive Members of other TF families also functioned in abiotic
MAPKcascadegenes(MAPK5andMAPKKK6),wellestablished stressresponsethroughROSregulation.ASRproteinsareplant-
salt-responsive TF genes (ZFP179 and DREB2A), and itself specific TFs and considered to be important regulators of
through direct interaction with the corresponding promoters plant response to various stresses. Wheat ASRgene, TaASR1, a
in plants (Schmidt et al., 2013). The authors proposed that positive regulator of plant tolerance to drought/osmotic stress,
FrontiersinPlantScience|www.frontiersin.org 8 December2015|Volume6|Article1092
YouandChan ROSRegulationinCropPlants
isinvolvedinthemodulationofROShomeostasisbyactivating indicatedthatOsSRO1chasdualrolesindroughtandoxidative
antioxidant system and transcription of stress-responsive genes stresstoleranceofricebypromotingstomatalclosureandH O
2 2
(Hu et al., 2013). Soybean NAC TF, GmNAC2, was identified accumulationthroughanovelpathwayinvolvingtheSNAC1and
asa negative regulator during abiotic stress,and participates in DSTregulators(Youetal.,2013).Recently,anSROgenewasalso
ROS signaling pathways through modulation of the expression identifiedtobecrucialforsalinitystressresistancebymodulating
ofgenesrelatedtoROS-scavenging(Jinetal.,2013).Ramegowda redoxhomeostasisinwheat(Liuetal.,2014).Ta-sro1,theallele
etal.(2012)isolatedastress-responsiveNACgene,EcNAC1,from of the salinity-tolerant bread wheat cultivar Shanrong No. 3, is
fingermillet(E.coracana).Transgenictobaccoplantsexpressing derivedfromthewheatparentalleleviapointmutation.Unlike
EcNAC1 increased ROS scavenging activity, up-regulated many Arabidopsis SRO proteins, Ta-sro1 has PARP activity. Both the
stress-responsivegenes,andexhibitedtolerancetovariousabiotic overexpressionofTa-sro1inwheatandArabidopsispromotesthe
stresses and MV-induced oxidative stress (Ramegowda et al., accumulationofROSbyregulatingROS-associatedenzyme.Ta-
2012). Recently, a NAC transcription factor gene, SNAC3, sro1 also enhances the activity of AsA-GSHcycle enzymes and
functions as a positive regulator under high temperature and GPX cycle enzymes, which regulate ROS content and cellular
droughtstress,wasidentifiedinrice(Fangetal.,2015).SNAC3 redoxhomeostasis(Liuetal.,2014).
enhances the abiotic stresses tolerance by modulating H O
2 2
homeostasis state through controlling the expression of ROS-
ROS-scavenging or Detoxification
associatedenzymegenes(Fangetal.,2015).
Proteins
In addition to TFs, transcriptional coregulator as well as
spliceosome component, OsSKIPa, a rice homolog of human Reactive oxygen species-scavenging enzymes such as SOD,
Ski-interacting protein (SKIP), has been studied for effects on APX, CAT were properly described its role in ROS-scavenging
drought resistance (Hou et al., 2009). OsSKIPa-overexpressing pathway.Thepresence ofantioxidant enzymesandcompounds
riceexhibited significantly enhanceddrought stresstolerance at in almost all cellular compartments suggests the importance of
both the seedling and reproductive stages by increased ROS- ROSdetoxificationforprotectionagainstvariousstresses(Mittler
scavenging ability and transcript levels of many stress-related et al., 2004). The effect of these ROS-scavenging enzymes in
genes(Houetal.,2009). abiotic stress resistance was also investigated in crop plants.
Transgenic alfalfa expressing MnSOD cDNA from Nicotiana
plumbaginifolia improved survival and vigor after exposure
SRO PROTEINS to water deficit. Most importantly, transgenic alfalfa showed
increased yield and survival rate over three winters in natural
TheSRO(SIMILARTORCDONE)proteinfamilywasrecently fieldenvironments(McKersie etal.,1996).AcDNAencodinga
identified as a group of plant-specific proteins, and they are cytosolic copper-zinc SOD from the mangrove plant Avicennia
characterized by the plant-specific domain architecture which marina was transformed into rice. The transgenic plants
contains a poly (ADP-ribose) polymerase catalytic (PARP) exhibitedmoretoleranttodrought,salinityandoxidativestresses
and a C-terminal RCD1-SRO-TAF4 (RST) domain (Jaspers compared with the untransformed control plants (Prashanth
et al., 2010). In addition to these two domains, some SRO etal.,2008).Overexpressionof OsAPX2increased APXactivity
proteins have an N-terminal WWE domain. Our limited and reduced H O and malondialdehyde (MDA) levels in
2 2
knowledge of SRO proteins is mainly from the study in transgenic plants under stress treatments (Zhang et al., 2013).
Arabidopsis mutant rcd1 (radical-induced cell death 1). rcd1 More importantly, OsAPX2-overexpressing plants were more
exhibits pleiotropic phenotypes related to a wide range of tolerant to drought stress than wild-type plants at the booting
exogenous stimulus responses and developmental processes, stage as indicated a significantly increase in spikelet fertility
includingsensitivitytoapoplasticROSandsaltstress,resistance under abiotic stresses (Zhang et al., 2013). Transgenic rice
to chloroplastic ROS caused by methyl viologen (MV) and plants that overexpressing another APX gene, OsAPX1, also
UV-B irradiation (Ahlfors et al., 2004; Fujibe et al., 2004; exhibitedincreasedspikeletfertilityundercoldstress(Satoetal.,
Katiyar-Agarwal et al., 2006). RCD1 interacts with SOS1 and 2011).
a large number of transcription factors which have been Accumulation of toxic products from ROS with lipids and
identified or predicted to beinvolved in both developmentand proteins significantly contributes to the damage of crop plants
stress-related processes (Katiyar-Agarwal et al., 2006; Jaspers under biotic and abiotic stresses. A novel plant NADPH-
et al., 2009). Recent study demonstrated that RCD1 is possibly dependent aldose/aldehyde reductase, which has the reduction
involvedinsignalingnetworksthatregulatequantitativechanges activity toward toxic products of lipid peroxidation, was
in gene expression in response to ROS (Brosche et al., isolated from alfalfa. Tobacco plants overproducing the alfalfa
2014). aldose/aldehyde reductase showed lower concentrations of
In rice, an SRO protein, OsSRO1c, was characterized as a reactivealdehydes(productsoflipidperoxidation)andtolerance
direct target of the drought stress-related transcription factor tooxidativeanddroughtstress(Oberschalletal.,2000).
SNAC1 (You et al., 2013). OsSRO1c was induced in guard Metallothioneins(MTs)areagroupoflowmolecularweight
cells by drought stress. Overexpression of OsSRO1c resulted in proteins with the characteristics of high cysteine (Cys) residue
accumulated H O in guard cells, which, in turn, decreased content and metal-binding ability. The presence of several Cys
2 2
stomatal aperture and reduced water loss. Further experiments residuesinMTssuggeststheirinvolvementinthedetoxification
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YouandChan ROSRegulationinCropPlants
of ROS or in the maintenance of redox levels. OsMT1a, Huda et al. (2013) report the isolation and characterization of
encoding a type 1 MT in rice, was induced by dehydration OsACA6,whichencodesamemberofthetypeIIBCa2+ATPase
and Zn2+ treatment (Yang et al., 2009). Transgenic rice plants family from rice. Overexpression of OsACA6 confers tolerance
overexpressingOsMT1aenhancedantioxidantenzymeactivities to salinity and drought stresses in tobacco, which was
of CAT, POD and APX, and enhanced tolerance to drought. correlated with reduced accumulation of ROS and enhanced
OsMT1a also regulates the expression of several zinc finger the expression of stress-responsive genesinplants (Huda etal.,
transcription factors by the modulation of Zn2+ homeostasis, 2013). In addition, overexpression of OsACA6 confers Cd2+
whichleadstoenhancedplantstresstolerance(Yangetal.,2009). stress tolerance in transgenic lines by maintaining cellular ion
GhMT3a encodes a type 3 plant MT in cotton. Recombinant homeostasis and modulating ROS-scavenging pathway (Shukla
GhMT3a protein showed an ability to bind metal ions and et al., 2014). Annexins are calcium-dependent, phospholipid-
scavenge ROS in vitro. Transgenic tobaccos showed more binding proteins with suggested functions in response to
tolerancetomultipleabioticstresses,andlowerH O levelswhen environmental stresses and signaling during plant growth and
2 2
compared with wild-type plants(Xueetal.,2009).TheSbMT-2 development. OsANN1, a member of the annexin protein
genefromahalophytewasalsoinvolvedinmaintainingcellular family in rice, has ATPase activity, the ability to bind Ca2+,
homeostasis by regulating ROS scavenging during stresses and and the ability to bind phospholipids in a Ca2+-dependent
thusimprovedtolerancetosaltandosmoticstressintransgenic manner.OsANN1confersabioticstresstolerancebymodulating
tobacco(Chaturvedietal.,2014). antioxidantaccumulationandinteractingwithOsCDPK24(Qiao
etal.,2015).
ABA Metabolic-related Proteins
Other Functional Proteins
Abscisic acid is a key phytohormone that medicates the
Polyaminesarelowmolecularweightaliphaticaminesfoundin
adaptive responses to abiotic stresses of plants. ABA-induced
all living cells. Because of their cationic nature at physiological
antioxidant defense has been well documented in plants. ABA
pH, PAs have strong binding capacity to negatively charged
biosynthesisandcatabolismalsoinvolvedinantioxidantdefense
molecules (DNA, RNA, and protein), thus stabilizing their
and abiotic stresses. Du et al. (2010) isolated a rice drought-
structure (Alcazar et al., 2010). The PAs biosynthetic pathway
sensitivemutantdsm2,impairedinthegeneencodingaputative
β-carotene hydroxylase. β-carotene hydroxylase ispredicted for has been thoroughly investigated in many organisms, and
arginine decarboxylase (ADC) plays a predominant role in the
the biosynthesis of zeaxanthin, a carotenoid precursor of ABA.
accumulationof PAsunderstresses(Capelletal.,2004;Alcazar
Underdroughtstress,dsm2mutantshadreducedzeaxanthinand
etal.,2010).Wangetal.(2011)isolatedanargininedecarboxylase
ABA, lower Fv/Fm and non-photochemical quenching (NPQ)
gene (PtADC) from Poncirus trifoliata. The transgenic tobacco
capacity than the wild type. Overexpression of DSM2 in rice
and tomato plants elevatedendogenous PAs level,accumulated
increasesthexanthophyllsandNPQcapacity,stress-relatedABA-
less ROS and showed an improvement in drought tolerance.
responsivegenesexpression,andresultedinenhancingresistance
Jang et al. (2012) identified a highly oxidative stress-resistant
todroughtandoxidativestresses(Duetal.,2010).OsABA8ox3,
(cid:2) T-DNA mutant line carried an insertion in OsLDC-like 1 in
encoding ABA 8-hydroxylase involved in ABA catabolism, is
rice.ThemutantproducedmuchhigherlevelsofPAscompared
alsoakeygeneregulatingABAaccumulationandanti-oxidative
to the wild type plants. Based on their results, the authors
stress capability under drought stress (Nguyen et al., 2015).
suggestedthatPAsmediatetolerancetoabioticstressesthrough
OsABA8ox3 RNAi plants exhibited significant improvement
their ability to decrease ROS generation and enhance ROS
in drought stress tolerance. Consistent with this, OsABA8ox3
degradation.
RNAi plants showed increased SOD and CAT activities and
The12-oxo-phytodienoicacidreductases(OPRs)areclassified
reduced MDA levels during dehydration treatment. In another
into two subgroups, OPRI and OPRII. OPRII proteins are
study, overexpression of the 9-cis-epoxycarotenoid dioxygenase
involvedinjasmonicacidsynthesis,whilethefunctionofOPRI
gene from Stylosanthes guianensis (SgNCED1) in the transgenic
isasyetunclear.Dongetal.(2013)characterizatedthefunctions
tobacco increased ABA content and tolerance to drought and
of the wheat OPRI gene TaOPR1. Overexpression of TaOPR1
salt stresses (Zhang et al., 2009). Moreover, enhanced abiotic
in wheat and Arabidopsis enhanced tolerance to salt stress by
stresses tolerance in transgenic plants is associated with ABA-
regulating of ROS and ABA signaling pathways (Dong et al.,
induced production of H O and NO, which, in turn, activate
2 2
2013).
theexpressionandactivitiesofROS-scavengingenzymes(Zhang
Helicasesareubiquitousenzymesthatcatalyzetheunwinding
etal.,2009).
ofenergeticallystableduplexDNAorRNAsecondarystructures,
and thereby play an important role in almost all DNA and/or
Calcium Transporters and
RNA metabolic processes. OsSUV3, an NTP-dependent
Calcium-binding Proteins
RNA/DNA helicase in rice, exhibits ATPase, RNA and
Calcium(Ca2+)regulatesnumeroussignalingpathwaysinvolved DNA helicase activities (Tuteja et al., 2013). OsSUV3 sense
in growth, development and stress tolerance. The influx of transgenicriceplantsshowedlesserlipidperoxidationandH O
2 2
Ca2+ into the cytosol is countered by pumping Ca2+ out production,alongwithhigheractivitiesofantioxidantenzymes,
from the cytosol to restore the basal cytosolic level, and this consequently resulting in increased tolerance to high salinity
may be achieved either by P-type Ca2+ATPases or antiporters. (Tutejaetal.,2013).
FrontiersinPlantScience|www.frontiersin.org 10 December2015|Volume6|Article1092