全 文 ：植物细胞活性氧种类、代谢及其信号转导?
许树成1 , 2 , 丁海东2 , 桑建荣2
( 1 阜阳师院生物系 , 安徽 阜阳 236032; 2 南京农业大学生命科学学院 , 江苏 南京 210095 )
摘要 : 越来越明显的证据表明 , 植物体十分活跃的产生着活性氧并将之作为信号分子、进而控制着诸如细
胞程序性死亡、非生物胁迫响应、病原体防御和系统信号等生命过程 , 而不仅是传统意义上的活性氧是有
氧代谢的附产物。日益增多的证据显示 , 由脱落酸、水杨酸、茉莉酸与乙烯以及活性氧所调节的激素信号
途径 , 在生物和非生物胁迫信号的“交谈”中起重要作用。活性氧最初被认为是动物吞噬细胞在宿主防御
反应时所释放的附产物 , 现在的研究清楚的表明 , 活性氧在动物和植物细胞信号途径中均起作用。活性氧
可以诱导细胞程序性死亡或坏死、可以诱导或抑制许多基因的表达 , 也可以激活上述级联信号。近来生物
化学与遗传学研究证实过氧化氢是介导植物生物胁迫与非生物胁迫的信号分子 , 过氧化氢的合成与作用似
乎与一氧化氮有关系。过氧化氢所调节的下游信号包括钙“动员”、蛋白磷酸化和基因表达等。
关键词 : 活性氧 ; MAPK ; H2 O2 ; 信号转导 ; 胁迫
中图分类号 : Q 945 文献标识码 : A 文章编号 : 0253 - 2700 (2007) 03 - 355 - 11
Reactive Oxygen Species, Metabolism , and Signal
Transduction in Plant Cells
XU Shu-Cheng
1 , 2
, DING Hai-Dong
2
, SANG Jian-Rong
2
(1 Depatment of Biology, Fuyang Teachers College, Fuyang 236032 , China;
2 Collegeof LifeSciences, Nanjing Agricultural University, Nanjing 210095 , China)
Abstract: Traditionally, reactive oxygen species ( ROS) were considered to be toxic by - products of aerobic metabolism .
However, in recent years, it has become apparent that plants actively produce ROS as signalingmolecules to control pro-
cesses such as programmed cell death, abiotic stress responses, pathogen defense and systemic signaling . Emerging evi-
dence suggests that hormone signaling pathways regulated by abscisic acid, salicylic acid, jasmonic acid and ethylene, as
well as ROS signaling pathways, playkey rolesin thecrosstalk between biotic and abioticstresssignaling . Reactiveoxygen
species (ROS) were originally thought to only be released by phagocytic cells during their role in host defence . It is now
clear that ROS have a cell signalling role in many biological systems, both in animals and in plants . ROS induce pro-
grammed cell death or necrosis, induce or suppress the expression of many genes, and activate cell signalling cascades,
such as those involving . Recent biochemical and genetic studies confirmthat hydrogen peroxide is a signallingmolecule in
plants that mediates responses to abiotic and biotic stresses . The synthesis and action of hydrogen peroxide appear to be
linked to those of nitric oxide . Downstreamsignalling events that aremodulated by hydrogen peroxide include calciummo-
bilization, protein phosphorylation and geneexpression .
Key words: ROS; MAPK ; H2 O2 ; Signal transduction; Stress
Ever since the introduction of molecular oxygen
(O2 ) into our atmosphereby O2 -evolving photosynthet-
ic organisms ～2 .7 billion years ago, reactive oxygen
species ( ROS) have been the unwelcome companions
of aerobic life ( Halliwell and Gutteridge, 1989 ) . In
contrast to O2 , these partially reduced or activated de-
云 南 植 物 研 究 2007 , 29 (3) : 355～365
Acta Botanica Yunnanica

? ?基金项目 : 安徽省教育厅科研资助项目 ( 2005KJ191)
Received date: 2006 - 09 - 05 , Accepted date: 2006 - 03 - 18
作者简介 : 许树成 (1969 - ) 男 , 博士 , 讲师 , 主要从事植物逆境生理与细胞生物学研究。E-mail : xscjack@tom. com
rivativesof oxygen such as singlet oxygen (1 O2 ) , su-
peroxide radical anion ( O2 - ) , hydrogen peroxide
(H2 O2 ) and hydroxyl radical (HO· ) are highly reac-
tive and toxic, and can lead to theoxidativedestruction
of cells (Asada and Takahashi , 1987 ) . (Fig . 1)
There aremany potential sourcesof ROS in plants
(Table 1 ) . Some are reactions involved in normal me-
tabolism, such as photosynthesis and respiration .
These are in line with the traditional concept, consid-
ering ROS as unavoidable byproducts of aerobic me-
tabolism (Asada and Takahashi , 1987 ) . Other sources
of ROS belong to pathways enhanced during abiotic
stresses, such as glycolate oxidase in peroxisomes dur-
ing photorespiration . However, in recent years, new
sources of ROS have been identified in plants, includ-
ing NADPH oxidases, amine oxidases and cell-wall-
bound peroxidases . These are tightly regulated and par-
ticipate in the production of ROS during processes such
as programmed cell death ( PCD ) and pathogen de-
fense ( Dat et al . 2000; Grant and Loake, 2000;
Hammond-Kosack and Jones, 1996) .
Consequently, the evolution of all aerobic organ-
isms has been dependent on the development of effi-
cient ROS-scavenging mechanisms . In recent years, a
new role for ROS has been identified: the control and
regulation of biological processes, such as growth, cell
cycle, programmed cell death, hormone signaling, bi-
otic and abiotic stress responses and development (Cos-
ta and Moradas-Ferreira, 2001; Foreman et al . 2003;
J iang et al . 2003; Kovtun et al . 2000; Kwak et al .
2003; Pei et al . 2000; Mullineaux and Karpinski ,
2002; Mittler, 2004; Neill et al . 2002; Overmyer et
al . 2003; Torres et al . 2002 ) . These studies extend
our understanding of ROS and suggest a dual role for
ROS in plant biology as both toxic byproducts of aero-
bic metabolism and key regulators of growth, develop-
ment and defense pathways . The useof ROS as signal-
ing molecules by plant cells suggests that during the
courseof evolution, plants were able to achieve a high
degreeof control over ROS toxicity and are now using
ROS as signaling molecules . Controlling ROS toxicity
while enabling ROS such as H2 O2 or O2
- to act as sig-
naling molecules appears to require a large gene net-
work composed of at least 152 genes in Arabidopsis
(Mittler, 2004) .
Biotic Strategies to Generate ROS
Oneof the most rapid defense reactions to patho-
gens attack is theso-calledoxidativeburst, which con-
stitutes the production of ROS, primarily superoxide
Fig . 1 Generation of different ROS by energy transfer or sequential
univalent reduction of ground state triplet oxygen .
Table 1 Producing, scavenging and avoiding reactive oxygen species in plants
Mechanism Localization Primary ROS Mechanism Localization Primary ROS
ROS Production Glutathione peroxidase Cyt H2 HO2 , ROOH
Photosynthesis ET and PSI or II Chl O2 M
- Peroxidases CW, Cyt, Vac H2 HO2
Respiration ET Mit O2 M
- Thioredoxin peroxidase Chl , Cyt, Mit H2 HO2
Glycolateoxidase Per H2 PO2 Ascorbic acid Chl , Cyt,Mit, Per, Apo H2 HO2 , O2
-
Excited chlorophyll Chl O2 M
1 Glutathione Chl , Cyt,Mit, Per, Apo H2 HO2
NADPH oxidase PM O2 M
- α-Tocopherol Membranes ROOH , O2 V1
Fatty acidβ-oxidation Per H2 PO2 Caretenoids Chl O2 E1
Oxalate oxidase Apo H2 PO2 Avoidance
Xanthine oxidase Per O2 M
- Anatomical adaptations Leaf structure, epidermis O2 9
-
,H2O2 ,O2
1
Peroxidases, Mn2 ?+ and NADH CW H2 NO2 , O2
- C4 5or CAM metabolism Chl , Cyt, Vac O2 E
-
, H2 O2
Amine oxidase Apo H2 PO2 Chl movement Cyt O2 9
-
,H2O2 ,O2
1
ROS Scavenging Suppression of photosynthesis Chl O2 E
-
, H2 O2
Superoxide dismutase Chl , Cyt,Mit, Per, Apo O2 M
- PS and antenna modulations Chl O2 E
-
, O2
1
Ascorbate peroxidase Chl , Cyt,Mit, Per, Apo H2 PO2 Alternative oxidases Chl , Mit O2 E
-
Catalase Per H2 PO2
Abbreviations: Apo, apoplast; Chl , chloroplast; CW, cell wall ; Cyt, cytosol ; ET, electron transport; Mit, mitochondria; O21 , singlet oxygen; Per,
peroxisome; PM, plasma membrane; PS, photosystem; ROI , reactiveoxygen intermediate; Vac, vacuole .
653 云 南 植 物 研 究 29 卷
and H2 O2 , at the site of attempted invasion ( Apostol
et al . 1989 ) . Several enzymes are now recognized as
being potentially able to produce ROS, perhaps the
most important of these is NADPH oxidase . The NAP-
DH-dependent oxidase system, similar to that present
inmammalianneutrophils, has received themost atten-
tion . In animals theNADPH oxidase is found in phago-
cyte and B lymphocytes . It catalyzes the production of
superoxideby the one-election reduction of oxygen us-
ing NADPH as the election donor .
In addition to the NADPH oxidase of phagocytes,
other NADPH oxidases also associated with plasma
membranes are found in a variety of cells ( Babior,
1999) . Morestudies haveprovided several linesof evi-
dence strongly suggesting a common origin for both
mammalian NADPH oxidases and plant NADPH oxidas-
es . Antibodies raised against human NADPH oxidases
subunits p22PHOX , p47PHOX , and p67PHOX cross-reacted
with plant proteins of similar size ( Desikan et al .
1996; Tenhaken et al . 1995 ) , and in several plant
species rboh genes ( respiratory burst oxidase homo-
logues) of p91PHOX , thecatalytic subunitof theNADPH
oxidases of phagocytes, have been found (Keller et al .
1998; Torres et al . 1998 ) . In addition to aplant spe-
cific NADPH oxidase, alternative mechanisms of ROS
production have been proposed . For example, many
peroxidases are localized in the apoplastic space and
are ionically or covalently bound to cell wall polymers .
Peroxidases can act in two different catalytic modes . In
thepresenceof H2 O2 andphenolic substrates they oper-
ate in the peroxidatic cycle and are engaged in the syn-
thesis of lignin and other phenolic polymers . Compared
with the plant, NADPH-oxidase activity that gives rise
to superoxide and hydrogenperoxide, invitro studiesof
horseradish peroxidase suggest another activity of this
enzyme: generating hydroxyl radicals ( Chen and
Schopfer, 1999 ) . Similar to the Fe2 +?3 + catalyzed
Haber-Weiss reaction, horseradish peroxidase can re-
duce hydrogen peroxide to hydroxyl radicals ( Chen and
Schopfer, 1999) .
Whereas, under normal growth conditions, the
production of ROS in cells is low (240μM s- 1 O2- and
a steady-state level of 0 .5 μM H2 O2 in chloroplasts
(Polle, 2001) , many stresses that disrupt the cellular
homeostasis of cells enhance the production of ROS
(240 - 720μM s- 1 O2 - and asteady-state level of 5 - 15
μM H2 O2 in chloroplasts) ( Polle, 2001 ) . These in-
clude drought stress and desiccation, salt stress, chill-
ing, heat shock, heavymetals, ultravioletradiation, air
pollutants such as ozone and SO2 , mechanical stress,
nutrient deprivation, pathogen attack and high light
stress (Allen, 1995; Bowler et al . 1992; Dat et al .
2000; Desikin et al . 2001; Pei et al . 2000; Noctor
and Foyer, 1998; Orozco-Cardenas and Ryan, 1999) .
The production of ROS during these stresses results
from pathways such as photorespiration, from the pho-
tosynthetic apparatus and from mitochondrial respira-
tion . In addition, pathogens and wounding or environ-
mental stresses ( e.g . drought or osmotic stress) have
been shown to trigger the active production of ROS by
NADPH oxidases ( Hammond-Kosack andJones, 1996;
Pei et al . 2000; Orozco-Cardenas and Ryan, 1999;
Cazale et al . 1999) .
Abiotic Strategies to Generate ROS
In plants, ROS are continuously produced pre-
dominantly in chloroplasts, mitochondria, and peroxi-
somes . Production and removal of ROS must bestrictly
controlled . However, the equilibrium between produc-
tion and scavenging of ROS may be perturbed by a
number of adverse abiotic stress factors such as high
light, drought, low temperature, andmechanical stress
(Field et al . 1998; Malan et al . 1990; Prasad et al .
1994; Tsugane et al . 1999 ) .
Chloroplasts hydrogen peroxide?superoxide
Oxygen is continuously produced during light-driv-
en photosynthetic electron transport and simultaneously
removed fromchloroplastsby reduction and assimilation .
There are three types of oxygen-consuming processes
closely associated with photosynthesis: ( a) the oxygen-
ase reaction of ribulose-1 , 5-bisphosphate carboxylase
(Rubisco) , (b) direct reaction of molecular oxygen by
photosystemⅠ (PSⅠ) electron transport, and (c) chloro-
respiration (Keller et al . 1998) . (Fig . 2)
Mitochondria as ROS sources (Kirk, 2003)
For years, the chloroplast was considered to be the
main sourceof ROS production in plant cells and conse-
quently one of the main targets for ROS damage during
stress . However, it has recently been suggested that the
chloroplast is not as sensitive to ROS damage as previ-
ously thought (Torres et al . 1998) . The mitochondrion
is another cellular siteof ROS production . However, re-
cent studies suggest that themitochondrion is also akey
regulator of PCD inplants and that enhanced ROS levels
7533 期 XU Shu-Cheng et al .: Reactive Oxygen Species, Metabolism, and Signal Transduction in Plant Cells
at the mitochondria can trigger PCD ( Torres et al .
2002) . The mitochondrial electron transport chain can
producesignificant quantities of ROS, primarily because
of the presence of the ubisemiquinone radical , which
can transfer a single electron to oxygen and produce
O2
-
. The mitochondrial alternative oxidase (AOX) ca-
talyses theO2 dependent oxidationof ubiquinol , limiting
themitochondrial generationof ROS . (Fig . 2)
Fig . 2 Differences in thesteady-state levels of reactiveoxygen intermed-
iates ( ROI ) during biotic stress and abiotic stress . Biotic stress ( a) re-
sults in the activation of NADPH oxidase and the suppression of ascorbate
peroxidase ( APX ) and catalase ( CAT ) . This leads to theover-accumula-
tion of ROI and the activation of defense mechanisms . Abiotic stress ( b)
enhances ROI production by chloroplasts and mitochondria . However, by
inducing ROI-scavenging enzymes such as APX and CAT, it reduces ROI
levels . Thequestion mark indicates that little is known about the regula-
tion of ROI metabolism during a combination of bioticand abiotic stresses .
Chloroplasts are indicated in upper, and mitochondria are in down .
ROS detoxification
Because ROS are toxic but also participate in sig-
naling events, plant cells require at least two different
mechanisms to regulate their intracellular ROS concen-
trations by scavengingof ROS: one that will enable the
finemodulation of low levels of ROS for signaling pur-
poses, andone that will enablethe detoxificationof ex-
cess, especially duringstress . In addition, thetypesof
ROS produced and thebalancebetween thesteady-state
levels of different ROS can also be important . These
aredetermined by the interplay between different ROS-
producing and ROS scavenging mechanisms, and can
change drastically depending upon the physiological
condition of the plant and the integration of different
environmental , developmental and biochemical stimuli .
In the presence of transition metal ions hydrogen
peroxidemay be reduced to hydroxyl radicals by super-
oxide . Superoxide and hydrogen peroxide aremuch less
reactive than OH . , then the main risk for a cell that
produces the two former reactive oxygen intermediates
may be posed by the two intermediates interaction,
leading to the generaction of highly reactive hydroxyl
radicals . Because there are no known scavengers of
hydroxyl radicals, theonly way to avoid oxidativedam-
agethrough this radical is to control the reactions that
lead to its generation . Thus, cells had to evolve so-
phisticated strategies to keep the concentrations of su-
peroxide, hydrogen peroxide, and transition metals
such as Fe and Cu under tight control .
Nonenzymatic ROS Scavenging Mechanisms
The first pathway to scavenge ROS is nonenzymatic
ROS scavenging . Nonenzymatic antioxidants in plant cells
include themajor cellular redox buffers ascorbateandglu-
tathione (GSH) , as well as tocopherol , flavonoids, alka-
loids, and carotenoids . Mutants with decreased ascorbic
acid levels (Keller et al . 1998) or altered GSH content
(Kirk, 2003) are hypersensitive to stress . Whereas GSH
is oxidized by ROS forming glutathione ( GSSG ) ,
ascorbate is oxidized to monodehydroascorbate (MDA)
and dehydroascorbate (DHA) (Table 1) .
Enzymatic ROS Scavenging Mechanisms
The secondpathway to scavengeROS is enzymatic
ROS scavenging . Enzymatic ROS scavenging mecha-
nisms in plants include superoxide dismutase (SOD) ,
ascorbate peroxidase ( APX ) , glutathione peroxidase
(GPX) , and catalase (CAT) (Table 1) .
The role of ROS in signal transduction
Recent studies have identified several components
involved in the signal transduction pathway of plants
that senses ROS . These include the mitogen-activated
protein (MAP) kinase kinase kinases AtANP1 and Nt-
NPK1, and the MAP kinases AtMPK3?6 and Ntp46MAPK
(Kovtun et al . 2000; Samuel et al . 2000) . In addition,
calmodulin has been implicated in ROS signaling (Desikin
et al . 2001; Harding et al . 1997) . A hypothetical mod-
el depicting some of the players involved in this path-
way is shown in Fig . 3 . and in Fig . 4 . H2 O2 is sensed
by a sensor that might be a two-component histidineki-
nase, as in yeast (Desikin et al . 2001 ) . Calmodulin
and aMAP-kinasecascade are then activated, resulting
in the activation or suppression of several transcription
factors . These regulate the response of plants to oxida-
tive stress ( Desikin et al . 2001; Maleck et al .
2000) . Cross-talk with the pathogen-response signal
transduction pathway also occurs and might involve in-
teractions between different MAP-kinase pathways,
feedback loops and the action of NO and SA as key
hormonal regulators . This model ( Fig . 3 and Fig . 4)
is simplified and is likely to change as research advanc-
853 云 南 植 物 研 究 29 卷
es our understanding of this pathway . ROS act as sig-
nals that mediate the systemic activation of gene expres-
sion in response to pathogen attack ( Alvarez et al .
1998) , wounding ( Orozco-Cardenas and Ryan, 1999 )
and high light (Mullineauxand Karpinski , 2002) .They
were suggested to act in conjunction with a compound
that travels systemically and activates their production
in distal parts of the plant, where they mediate the in-
duction of gene expression ( Orozco-Cardenas and Ry-
an, 1999) . The involvement of ROS in the regulation
of stomatal closure (Pei et al . 2000) and in other cel-
lular responses involving auxin ( Kovtun et al . 2000;
Klaus and Heribert, 2004 ) might suggest that more
signaling pathways involving ROS as inducers of sys-
temic signals await discovery . It is unlikely that ROS
can travel systemically because they are highly reactive
and wouldbe scavenged along theway by themany an-
tioxidative mechanisms and antioxidants present in the
apoplast . However, it is possiblethat awaveof activity
similar to the‘oxidative burst’ is activated in cells
along the systemic path and in distal tissues, resulting
in the accumulation of ROS . Future studies using pla-
nts with altered levels of ROS-scavenging and?or ROS-
producing mechanisms might resolve this question .
Reactive oxygen species and hormonal network
Hormone signaling pathways govern biotic and abi-
otic stress responses through ROS
ABA is a phytohormone that is extensively in-
volved in responses to abiotic stresses such as drought,
low temperature, andosmotic stress . ABA also governs
a variety of growth and developmental processes, in-
cluding seed development, dormancy, germination, and
stomatal movement . By contrast, the phytohormones
SA , JA , and ET play central roles in biotic stress sig-
nalingupon pathogen infection . In many cases , ABA
Fig . 3 A suggestedmodel for the activation of signal transduction events during oxidative stress . H2 O2 is detected by a cellular receptor or sensor . Its de-
tection results in the activation of a Mitogen activated-protein kinase (MAPK ) cascade and agroup of transcription factors that control different cellular path-
ways . H2 O2 sensing is also linked to changes in the levels of Ca
2+ and calmodulin, and to the activation or induction of a Ca2 + -calmodulin kinase that can
also activateor suppress the activity of transcription factors . The regulation of gene expression by the different transcription factors results in the induction
of various defense pathways, such as reactive oxygen intermediate ( ROI ) scavenging and heat-shock proteins ( HSPs) , and in the suppression of some ROI-pro-
ducing mechanisms and photosynthesis . Thereisalso cross-talk with theplant-pathogensignal transduction pathway, which might depend on pathogenrecognition by
the gene-for-gene mechanismand can result in an inverse effect on the regulation of ROS-production and ROI-scavenging mechanisms, as well ason the activation
of programmed cell death (PCD) . The plant hormones nitric oxide (NO)、abscisic acid (ABA ) and salicylic acid (SA ) are key regulators of this response .
9533 期 XU Shu-Cheng et al .: Reactive Oxygen Species, Metabolism, and Signal Transduction in Plant Cells
Fig . 4 Schematic depiction of cellular ROS sensing and signalling mecha-
nisms . ROS sensors such as membrane-localized histidine kinases can
sense extracellular and intracellular ROS . Intracellular ROS can also influ-
ence the ROS-induced mitogen-activated protein kinase (MAPK ) signalling
pathway through inhibition of MAPK phosphates ( PPases) or downstream
transcription factors . WhereasMAP kinases regulategene expression by al-
tering transcription factor activity through phosphorylation of serine and
threonineresidues, ROS regulation occurs by oxidation of cysteineresidues .
acts as a negative regulator of disease resistance
(Mauch-Mani and Mauch, 2005 ) . For example, the
ABA-deficient tomato mutant sitiens has increased re-
sistance to pathogens and applicationof exogenous ABA
restored the susceptibility of sitiens (Audenaert et al .
2002; Thaler and Bostock, 2004) . The sitiens mutant
has greater SA-mediated responses, suggesting that
high ABA concentrations inhibit the SA-dependent de-
fense response in tomato . ABA and ET are well known
to interact, mostly antagonistically, in a number of de-
velopmental processes and in vegetative tissues ( Beau-
doin et al . 2000; Ghassemian et al . 2000) . Genetic
analysis of enhanced response to ABA3 ( era3) alleles
revealed that ERA3 is allelic to ETHYLENE INSENSI-
TIVE2 ( EIN2 ) , which encodes a membrane-bound
putative divalent cation sensor that may represent a
crosstalk point that intersects theABA and ET signaling
pathways ( Ghassemian et al . 2000 ) . Furthermore,
jasmonic acid resistance1 ( jar1 ) and jasmonic acid in-
sensitive4 ( jin4) mutants, which are hypersensitive to
ABA-mediated inhibitionof germination, exhibit antag-
onistic effects of ABA and JA ( Lorenzo and Solano,
2005; Anderson et al . 2004 ) . Additionally, exoge-
nous application of ABA resulted in the downregulation
of JA- or ET-responsive defense gene expression in
wildtype plants, whereas higher expression levels of
these defense genes were observed in ABA deficient
mutants without any treatments ( Anderson et al .
2004) . Taken together with the findings that exogenous
application of methyl-JA and ET cannot restore the de-
fensegene expression that is suppressed by exogenous
ABA application, these data suggest that the ABA-me-
diated abiotic stress response is a dominant process
(Anderson et al . 2004) .
Additionally, recent studies identified other mo-
lecular entities that significantly impact crosstalk among
stress responsepathwaysviahormonesignaling . For in-
stance, both nitric oxide ( Wendehenne et al . 2004)
and Ca
2 +
signaling play an important role in plant de-
fense responses, ABA-dependent stomatal movements,
and drought stress responses ( Ludwig et al . 2004 ) .
Calcium dependent protein kinases in tobacco might
control biotic and abiotic stress responses via signaling
pathways that are mediated by hormones such as SA ,
ET, JA , and ABA ( Ludwig et al . 2005; Chung et
al . 2004; Ludwig et al . 2004 ) . In addition, fungal
elicitors can activate a branch of the ABA signaling
pathway in guard cells that regulates plasma membrane
Ca2 + channels (Klusener et al . 2002) . Moreover, a
battery of studies examining the induction of resistance
by the non-protein amino acid b-aminobutyric acid re-
vealed that ABA considerably enhances plant resistance
to fungal pathogens through itspositive effect on callose
deposition ( Mauch-Mani and Mauch, 2005; Ton et
al . 2005; Ton and Mauch-Mani , 2004) (Fig . 5) .
Roles of ROS at points of convergence between bi-
otic and abiotic stress response pathways
The tight regulation of the steady-state levels of
ROS is involved in multiple cellular processes in plants
( Zhang and Klessig, 2001 ) . Some ROS species are
toxic byproducts of aerobic metabolism, whereas ROS
also function as signaling molecules ( Zhang and Kles-
sig, 2001) . Rapid ROS production plays a pivotal role
in both ABA signaling and disease resistance responses
(Guan et al . 2000; Laloi et al . 2004) . Several lines
of evidence suggests that the NADPH-dependent respir-
atory burst oxidase homologgenes ( AtrbohD and Atrbo-
hF ) are required for ROS generation, leading to ABA-
induced stomatal closure and to hypersensitive cell
death in response to avirulent pathogen attack (Kwak
et al . 2003; Torres and Dangl , 2005; Torres et al .
063 云 南 植 物 研 究 29 卷
2002) . ROS scavengers are thought to detoxify the cy-
totoxic effects of ROS under various stress conditions
(Klaus and Heribert, 2004; Mittler, 2004 ) . Large-
scale transcriptome analyses of plants that had been
subjected to various abiotic and biotic stress treatments
revealed the induction of a large set of genes that en-
code ROS-scavenging enzymes under these conditions
(Seki et al . 2002; Schenk et al . 2000; Mittler et al .
2004) . Moreover, scavenging enzymes (e.g . superox-
ide dismutase, glutathione peroxidase and ascorbate
peroxidase) have been utilized to engineer plants that
are tolerant of abiotic stresses ( Bartels and Sunkar,
2005; Umezawa et al . 2006) . Microarray analysis us-
ing Arabidopsis cultured cells reveal that many ABA
inducible genes are induced by oxidative stress ( Taka-
hashi et al . 2004 ) . Recently, it has been suggested
that aC2 H2 -typezincfinger transcription factor, Zat12 ,
might be a regulator in the ROS scavengingmechanism
that is involved in biotic and abiotic stress responses .
Deficiency in Zat12 , which ishighly responsiveto mul-
tiple stresses including wounding, pathogen infection
and abiotic stresses (Seki et al . 2002; Zimmermann
et al . 2004; Davletova et al . 2005; Vogel et al .
2005) , suppresses the expression of the ASCORBATE
PEROXIDASE 1 ( APX1) gene, which is induced by
H2 O2 and increases the level of H2 O2 -induced protein
oxidation ( Rizhsky et al . 2004 ) . Overexpression of
Zat12 results in upregulation of oxidative- and light-
stress-responsive genes and in enhanced tolerance of
high light, freezing, and oxidative stresses (Davletova
et al . 2005; Lida et al . 2000; Rizhsky et al . 2004;
Vogel et al . 2005; Zimmermann et al . 2004) . Inter-
estingly, theexpressionof Zat12 is regulated by a redox-
sensitive transcription factor, HEAT SHOCK FACTOR
(HSF) 21 , which is likely to be an initial sensor for
H2 O2 that accumulates in response to various stresses
(Davletova et al . 2005 ) . These findings suggest that
the ROS might mediate crosstalk between biotic and
abiotic stress-responsive gene-expression networks
(Fig . 5) .
Reactive oxygen species signaling networks of plants
ROS can bedetected by at least threemechanisms
( ROS receptors, redox sensitive transcription factors
and phosphatases) . Detection of ROS by receptors re-
sults in thegenerationof Ca
2 +
signals and theactivation
of aphospholipaseC?D (PLC?PLD) activity that gener-
ates phosphatidic acid (PA) . PA and Ca2 + are thought
to activate theproteinkinaseOXI1 . Activationof OXI1
results in the activation of a mitogen-activatedprotein
kinase (MAPK ) cascade (MAPK3?6) and the induction
or activation of different transcription factors that regu-
late the ROS-scavenging and ROS-producing pathways .
The activation or inhibition of redox-sensitive transcrip-
tion factors by ROS might also affect the expression of
Fig . 5 Convergence points in abiotic and biotic stress signaling networks .
1633 期 XU Shu-Cheng et al .: Reactive Oxygen Species, Metabolism, and Signal Transduction in Plant Cells
OXI1 or other kinases and?or the induction of ROS-
specifictranscription factors . Inhibition of phosphatases
by ROS might result in the activationof kinases such as
OXI1 or MAPK3?6 . Two different loops are shown to
be involved in the ROS signal transduction pathway . A
localizedor general defense response ( a negative feed-
back loop; solid green line) can be activated to sup-
press ROS, whereas a localized amplification loop
( positive feedback loop; red dashed line) can be acti-
vated to enhance ROS signals via the activity of NAD-
PH oxidases . Salicylic acid ( SA ) and nitric oxide
(NO) might be involved in this amplification loop as
enhancers . (Fig . 6) .
Fig . 6 Generalized model of the reactive oxygen species
( ROS) signal transduction pathway .
Abbreviations: HSF , heat shock factor; PDK , phosphoinositide-depen-
dent kinase; TF , transcription factor; SA , Salicylic; NO, nitric oxide .
Conclusions
During the evolution of organisms that are adapted
to aerobic lifeconditions, ROS seemto haveundergone
several modifications of their biological activities . The
continuous production of ROS, an unavoidable conse-
quenceof aerobic metabolic processes such as respira-
tion and photosynthesis, has necessitated the evolution
of ROS scavengers in order to minimise the cytotoxic
effects of ROS within the cell . Disturbances is used by
plants to activate stress responses that help the plant to
cope with environmental changes . Finally, the geneti-
cally controlled production of H2 O2 (e.g . by NADPH
oxidases) is apparently used by plants to release an in-
tracellular signal that, often together with nitric oxide,
controls avariety of processes (Guo et al . 2003; Neill
et al . 2002 ) . Detailed information on how these two
signalingmolecules interact andhow they are sensed are
still scarce . Key issues to be addressed in the future
concern the questionsof howROS are integrated into the
general signaling network of a cell , how the chemical
identity of a given ROS and?or its intracellular produc-
tion sites affect its signalling, and what factors deter-
mine the specificity of the biological activities of ROS .
For example, the roleof mitogen-activated protein
kinase (MAPK ) in abscisic acid (ABA ) -induced an-
tioxidant defense was investigated extensively in leaves
of maize ( Zea mays L .) plants . Treatments with ABA
or H2 O2 induced the activation of a 46 kDa MAPK and
enhanced the expressionof the antioxidant genes CAT1 ,
cAPX and GR1 and thetotal activitiesof the antioxidant
enzymes catalase (CAT ) , ascorbateperoxidase (APX) ,
glutathione reductase (GR ) and superoxide dismutase
(SOD) (Aying et al . 2006) .Thehistochemical and cy-
tochemical localization of abscisic acid (ABA) -induced
H2 O2 production in leaves of maize ( Zea maysL .) pla-
nts were examined (Xiu et al . 2005) .
Current evidence supports the concept that ROS
represent a significant point of convergence between
pathways that respond to biotic and abiotic stresses .
Nevertheless, our current understandingof ROS partic-
ipation in crosstalk between these pathways is very lim-
ited . Thus, dissecting the genetic network that regu-
lates ROS signaling in response to biotic and abiotic
stresses merits extensive future study . When com-
bined, the results of large-scale transcriptome, pro-
teome, and metabolome analyses in plants will enable
the elucidation of the ROS network components that
govern multiple stress signaling pathways . In particu-
lar, the Genevestigator software should yield powerful
clues, allowingus to connect these key molecular play-
ers and to discover novel crosstalk networks ( Zimmer-
mann et al . 2005 ) . A significant body of research
suggests an antagonistic interaction betweenABA-medi-
ated abiotic stress signaling and disease resistance .
This relationship may simply suggest that plants have
developed strategies to avoid simultaneously producing
proteins that are involved in abiotic stress and disease
resistance responses ( Anderson et al . 2004 ) . In na-
ture, simultaneous exposure of plants to drought and
necrotrophic pathogen attack is actually rare, as suc-
cessful pathogen infection requires relatively humid
conditions . The finding that high humidity and high
temperature weaken plant resistance to pathogen attack
is consistent with this concept . Moreover, theviewthat
the ABA mediated abiotic stress signaling potentially
takes precedenceover biotic stress signaling (Anderson
et al . 2004) also supports the notion that water stress
263 云 南 植 物 研 究 29 卷
more significantly threatens plant survival than does
pathogen infection . To date, the biological significance
of crosstalk betweensignalingpathways thatoperateun-
der stress conditions and the mechanisms that underlie
this crosstalk remain obscure . We are just beginning to
dissect key factors governing the crosstalk between
these signaling pathways under various stress condi-
tions .
Conclusions and future challenges
Powerful genetic strategies driven by the use of
Arabidopsis have resulted in the elucidation of many
hormone and other signaling pathways in plants . As il-
lustrated by the studies reviewed here, the application
of this knowledge and, in particular, the useof signal-
ing mutants have allowed the delineation of signals in-
volved in cell death regulation . Similarly, genetic ap-
proaches involvingmutants have been key in identifying
novel plant pathways, such as the MAP kinase cas-
cades involved in the regulation of ROS responses and
cell death regulation . The picture is also more compli-
cated, considering that even more hormones (e.g . ab-
scisic acid and gibberellic acid) are likely to be in-
volved in cell death regulation (Klusener et al . 2002;
Bethke et al . 1999) . Continued work with these pow-
erful systems should result in the further molecular def-
inition of these pathways and poses the challenge to
produce an integratedmap that connects thesepathways
at themolecular level .
Future challenges and questions
The cause of cell death induced in plants by oxi-
dative stress is not well known . Is it simply the toxicity
of ROS that damages cells or is it the activation of a
PCD pathway by ROS ? It is possible that the level of
H2 O2 that is currently thought to kill cells by direct
cellular damage actually induces PCD ( Lam et al .
2001; Mitsuhara et al . 1999) , and it might require a
higher level of ROS to kill cells by direct oxidation .
Perhaps future studies applying oxidative stress to mu-
tants deficient in different PCD pathways will answer
this question . Many questions related to ROS me-
tabolism remain unanswered . We are currently at an
exciting time, when most of the technologies required
to answer these questions are in place . Thus, a com-
prehensive analysis of gene expression using microar-
rays and chips, coupledwith proteomics and metabolo-
mics to follow different antioxidants and related com-
pounds during oxidative stress, should answer many of
thesequestions .This analysis canbeperformedonpla-
nts respondingto abiotic stresses, biotic insultsor com-
binations of both, and can be complemented by using
mutants with altered ability to produce or scavenge
ROS . In addition, the development of cellular markers
that enable thenondestructive quantificationof different
ROS in the different cellular compartments, like the
markers used for Ca2 + imaging, will considerably ad-
vanceour understandingof ROS metabolism .
Abbreviations : ABA : abscisic acid; AOX : alternativeoxidase;
AtMPK3: Arabidopsis thaliana MAPK3; AtNDPK2: Arabidopsis
thaliana NUCLEOTIDE DIPHOSPHATE KINASE2 ; MAPK : mi-
togen-activated protein kinase; 1 O2 : singlet oxygen; ost1: open
stomata1; PCD: programmed cell death; PR: pathogenesis-re-
lated; PTP: protein tyrosine phosphatases; Rboh: respiratory
burst oxidase homologue; ROS: reactive oxygen species; SA :
salicylic acid; NO: nitric oxide; JA : jasmonic acid; ET: eth-
ylene; TF: transcription factor; ABI1: ABA-INSENSITIVE1;
CaM : calmodulin; GA : gibberellin; H2 O2 : hydrogenperoxide;
PP : protein phosphatase
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