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PHYSIOLOGIA PLANTARUM 119: 355–364. 2003
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Copyright # Physiologia Plantarum 2003
Redox sensing and signalling associated with reactive oxygen
in chloroplasts, peroxisomes and mitochondria
Christine H. Foyera,* and Graham Noctorb
a
Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
Institut de Biotechnologie des Plantes, Bâtiment 630, Universite´ Paris XI, 91405 Orsay Cedex, France
*Corresponding author, e-mail: [email protected]
b
Received 4 February 2003; revised 19 May 2003
Chloroplasts and mitochondria are the powerhouses of photosynthetic cells. The oxidation-reduction (redox) cascades of
the photosynthetic and respiratory electron transport chains
not only provide the driving forces for metabolism but also
generate redox signals, which participate in and regulate every
aspect of plant biology from gene expression and translation
to enzyme chemistry. Plastoquinone, thioredoxin and reactive
oxygen have all been shown to have signalling functions.
Moreover, the intrinsic involvement of molecular oxygen in
electron transport processes with the inherent generation of
superoxide, hydrogen peroxide and singlet oxygen provides a
repertoire of additional extremely powerful signals. Accumulating evidence implicates the major redox buffers of plant
cells, ascorbate and glutathione, in redox signal transduction.
The network of redox signals from energy-generating organelles orchestrates metabolism to adjust energy production to
utilization, interfacing with hormone signalling to respond to
environmental change at every stage of plant development.
Introduction
All living organisms are oxidation–reduction (redox)
systems. They use anabolic, reductive processes to store
energy and catabolic, oxidative processes to release it.
Through photosynthesis, plants set this global wheel in
motion. By harnessing light energy to drive biochemistry,
photosynthetic organisms have perfected the art of redox
control. Redox signals are the most fundamental forms
of information monitored by photosynthetic organisms
(Noctor and Foyer 1998). These types of signals may
well belong to the earliest evolved controls since
they prevent uncontrolled ‘boom and bust’ scenarios in
energy availability, utilization and exchange. More
complex aspects of redox control of physiology through
regulation of gene expression developed with the
evolution of higher plants. It is now widely accepted
that redox signals are key regulators of plant metabolism, morphology and development, and it may even
be that all intermediates and other systems of signal
transduction arose around this central core. These signals exert control on nearly every aspect of plant biology
from chemistry to development, growth and eventual
death. Controlled production of reactive oxygen species
(ROS) acts as a second messenger, alongside other mediators such as calcium, not only in plant responses to
pathogens but also in hormone signalling (Pei et al.
2000). Recent developments have greatly increased our
understanding of how systems in organelles involved in
photosynthesis sense redox changes, particularly those
linked to reactive oxygen in order to regulate whole cell
redox homeostasis.
The key role of reactive oxygen species and
antioxidants in plant redox homeostasis
Photosynthetic and respiratory electron transport chains
are the primary energy-transducing processes in eukaryotic
organisms. The evolution of oxygenic photosynthesis,
Abbreviations – ABA, abscissic acid; APX, ascorbate peroxidase; DHA, dehydroascorbate; GPX, glutathione peroxidase; GRX,
glutaredoxin; GSH, reduced glutathione; GSSG, glutathione disulphide; GST, glutathione S-transferase; LHC, light-harvesting complex;
M-POX, Mehler-peroxidase; (i)NOS, (inducible) nitric oxide synthase; PQ, plastoquinone; PRX, peroxiredoxin; PSI, photosystem I; PSII,
photosystem II; ROS, reactive oxygen species; TRX, thioredoxin.
Physiol. Plant. 119, 2003
355
an event that occurred two billion years ago, provided
abundant oxygen and facilitated the elaboration of reactions involving O2, particularly aerobic respiration. Almost
all life is based on the essential energy exchange reactions of
photosynthesis and respiration. The evolution of photosystem II first allowed use of the very high electrochemical
potential (Em7 ¼ 1 815 mV) of the O2/H2O redox couple.
Oxygenic photosynthesis and aerobic respiration today deal
with concerted, four-electron exchange between water and
oxygen, without release of reactive, partially reduced intermediates. However, many processes in plants (and in other
organisms) catalyse only partial reduction of oxygen, and so
generate superoxide, H2O2, and hydroxyl radicals (Noctor
and Foyer 1998, Mittler 2002). In addition, a reaction
potentially common in the thylakoid pigment beds involves
photodynamic energy transfer to ground-state triplet O2
and leads to the formation of highly reactive singlet O2.
Redox signals are involved in all aspects of plant
biology. They are particularly important in defence
responses and cross-tolerance phenomena, enabling a
general acclimation of plants to stressful conditions.
H2O2 has long been recognized as a signal-transducing
molecule in the activation of defence responses in
plants. It mediates intra- and extra-cellular communication during plant reactions to pathogens and several
studies have suggested a role in systemic acquired resistance. The hypersensitive response (HR) is a widespread
phenomenon that is responsible for the activation and
establishment of plant immunity to disease. HR is an
example of plant programmed cell death as it leads
to rapid, localized cell death at infection sites. This
contributes to the limitation of the growth and spread
of the invading pathogen. One of the earliest events in
the HR is the rapid accumulation of ROS through the
activation of enzyme systems, some of which are similar
to neutrophil NADPH oxidase (Keller et al. 1998). The
oxidative burst is a central component of an integrated
HR signalling system, whose function is rapid amplification of the signal. Other signalling components involved
in HR are salicylic acid (SA) and cytosolic Ca21. H2O2
has a strong regulatory influence on fluxes through Ca21
channels and on Ca21 concentrations in different cellular
compartments. During HR, H2O2 is required to trigger
localized host cell death but it seems that NO is
also needed to induce an efficient cell death response
(Delledonne et al. 1998). Further evidence that the
H2O2 cascade interacts closely with other signalling
systems comes from studies on hormone-mediated
stomatal movement (Pei et al. 2000), cell growth (Rodriguez
et al. 2002) and tropic responses (Joo et al. 2001). Such
studies show that H2O2 is a common secondary messenger in hormone-mediated events.
ensure control of the cellular redox state rather than to
facilitate the complete elimination of H2O2 (Foyer and
Noctor 2000). The antioxidative system determines the
lifetime of H2O2 in planta. Plant cells are strongly redox
buffered and contain very large quantities of the soluble
hydrophilic antioxidants, ascorbate (10–100 mM) and
glutathione (0.2–10 mM) (Noctor and Foyer 1998,
Hartmann et al. 2003). Most of their intracellular compartments hence have the capacity to deal with even very
high fluxes of H2O2 production. Rapid compartmentspecific differences in redox state (and hence signalling)
that influence the operation of many fundamental processes in plants, can be achieved by modifying ROS
(particularly H2O2) production or by repression or
activation of antioxidant defences. Recent evidence suggests that glutathione and ascorbate are key components
of redox signalling in plants (Baier et al. 2000, Noctor
et al. 2000, Horling et al. 2003). Specific compartmentbased signalling and regulation of gene expression can be
achieved via differential compartment-based changes in
either the absolute concentrations of ascorbate and glutathione or the ascorbate/dehydroascorbate and GSH/
GSSG ratios, which are very high and stable in the
absence of stress (Noctor et al. 2000).
Three factors are particularly significant in governing
the importance of H2O2 in signalling redox status in a
given compartment. The first is the absolute rate of H2O2
production. Figure 1 shows rates of H2O2 production in
different compartments during photosynthesis at moderately high light and optimal temperatures. Photosynthesis produces superoxide as result of direct electron
transfer to oxygen, from which H2O2 is produced and
metabolized through the Mehler-peroxidase (M-POX)
reaction. Assuming, however, that the M-POX reaction
is not a sink for more than 10% of photosynthetic electron flow, H2O2 is probably produced even faster in the
peroxisomes, at least in C3 plants, by virtue of the glycollate oxidase reaction. The second important factor is the
rate of scavenging by detoxifying systems. These two factors are likely to be the main determinants of H2O2 concentration. Third, the probability of reaction of H2O2 with
signalling components is probably a key determinant of
signalling intensity. As we discuss below, early components
in redox signalling are likely to include antioxidants and/or
antioxidative enzymes. The influence of a given compartment in redox signalling may differ as a function of how
well primed each compartment is with sensing components,
the nature of the signal that these components sense (e.g.
H2O2 or other ROS, electron transport components,
organic peroxides), and to what extent sensing components
are coupled to downstream transduction factors such as
kinase cascades (Kovtun et al. 2000).
Rates of H2O2 production in different compartments
during C3 photosynthesis
Redox signalling from the chloroplast
Plants are more tolerant of H2O2 than animals, and their
antioxidant systems appear to have been designed to
356
The chloroplast is an excellent model for understanding
redox-regulated plant gene expression (Pfannschmidt
et al. 1999). The light-driven chemistry of photosynthesis
Physiol. Plant. 119, 2003
Chloroplast
Photorespiration
CO2 fixation
4030
nmol.m–2.s–1
Peroxisome
Mitochondrion
Electron
transport
chain
Glycolate
H2O2
Glyoxylate
H2O2
10000
nmol.m–2.s–1
NADH
TCA
cycle
Reductant
Shuttle
Electron
transport
chain
Electron
transport
Serine
Glycine
<182
nmol.m–2.s–1
NADH
H2O2
NADH
H2O2 DARK
LIGHT
<216
nmol.m–2.s–1
Fig. 1. Typical rates of H2O2 production in the organelles of mesophyll cells during C3 photosynthesis. Numerous other ROS-generating
reactions are not considered – the above processes are presumed to be the fastest ROS-generating reactions in photosynthetic cells, at least in
the absence of an oxidative burst at the plasmalemma. Values are necessarily approximate and are supposed to compare likely typical rates of
H2O2 production in the different compartments. These are derived using established models of C3 photosynthesis (eg. Noctor et al. (2002)), in
which TCA cycle activity in the light is taken to be 50% of the rate in the dark and 50% of the NADH produced by glycine decarboxylase is
oxidized by the mitochondrial electron transport chain. Rates of net photosynthetic CO2 assimilation (19 mmol m2 leaf surface s1) are taken
to be about 10 times faster than total respiratory O2 uptake in the dark (2 mmol m2 leaf surface s1). Chloroplastic and mitochondrial H2O2
production are calculated assuming likely upper limits of electron leakage to superoxide in optimal conditions (10% of total photosynthetic
electron flow and 5% of total respiratory electron flow – for further discussion, see Foyer and Noctor (2000)). Peroxisomal H2O2 production
through reactions other than glycollate oxidation is considered to be relatively minor in C3 leaves in the light, and is not considered.
consists of a series of redox steps involving structural
components or functionally coupled pools of redoxactive compounds, such as thioredoxin (TRX), ascorbate
and glutathione. Changes in the redox state of these
components regulate the expression of both plastomeand nuclear-encoded chloroplast proteins. This redox
information co-ordinates expression in both compartments (Allen and Pfannschmidt 2000). To date, genetic
and biochemical analysis has identified plastoquinone
(PQ), ROS, ascorbate and the ferredoxin/TRX system
as redox-active signalling components (Danon and
Mayfield 1994, Escoubas et al. 1995, Karpinski et al. 1997,
Pfannschmidt et al. 1999, Schürmann and Jacquot 2000,
Kiddle et al. 2003). There is little doubt that other redox
signalling molecules remain to be discovered. For example,
the membrane-bound peroxiredoxins (PRX), whose
main role may be protection against lipid peroxidation,
have all the necessary molecular characteristics of thiol
Physiol. Plant. 119, 2003
signal-transducing components. Thus far, redox signals
have been shown to control post-translational modification of proteins via phosphorylation, redox modulation
of assimilatory reactions and control of gene transcription and translation (Somanchi and Mayfield 1999, Link
1999, Pfannschmidt et al. 1999). Photosynthetic control
of gene expression can now be described for the genes
located in chloroplasts themselves, both at transcriptional and post-transcriptional levels (Pfannschmidt
et al. 1999). Redox signals also leave the chloroplast to
provide a decisive input into transcriptional control
in the cell nucleus. Allen (1993) suggested that redox
signalling is a key function of the cytoplasmic genomes
found in the chloroplast and mitochondria, with the
exchange of redox information between these organelles
and the nucleus functioning within the global network
regulating plastid and mitochondrial metabolism and
development.
357
Coupling of photosynthetic electron transport and
redox poise to the expression of genes encoding chloroplast proteins enables plants to respond to diverse environmental conditions. Of the latter, light quality and
quantity have been most intensely studied. The expression of plastid-encoded photosynthetic proteins is precisely co-ordinated with that of their nuclear-encoded
partners (Kettunen et al. 1997, Surpin and Chory
1997). The light-activated increases in chloroplast protein synthesis are governed by redox-modulated transcriptional and translational controls (Rochaix 1996).
For example, the activity of the psbA-RNA binding
protein complex is subject to redox-regulation, probably
via TRX (Danon and Mayfield 1994). In this system, the
flux of electrons through the electron transport chain
induces a change in the sulfhydryl status of TRX and
hence the RNP complex, thereby allowing binding to the
psbA mRNA and formation of a translation initiation
complex.
A second light-modulated system, which has been
described in detail, involves the reversible redox
activation of membrane protein kinases. The kinases
phosphorylate two distinct groups of proteins. The first
are the light-harvesting chlorophyll a/b antenna system
of PSII. The reversible activation of the light-harvesting
antenna complex II (LHCII) kinase(s) is related to
the regulation and optimization of energy transfer
between PSII and PSI. Activation of the LHCII protein
kinase occurs via dynamic conformational changes in the
cytochrome b6f complex taking place during plastoquinol oxidation. De-activation of the kinase involves
its re-association with an oxidized cytochrome complex.
Maximal phosphorylation of components such as Lhcb1
and Lhcb2 proteins is only observed at irradiances far
below those experienced by the leaves during growth.
Such observations are explained by the presence of a
redox (probably TRX)-dependent regulatory loop that
inhibits the activation of the kinase at high light via
reduction of protein disulphide groups (Gal et al. 1997).
Recently, a thylakoid protein kinase with these properties has been cloned from Chlamydomonas (Depège et al.
2003). The second group of phosphorylated thylakoid
proteins are the PSII core proteins (D1 and D2 reaction
centre proteins, CP43 internal antenna protein and the
9 kDa psbH gene product). However, it is noteworthy
that the thylakoid protein kinase that phosphorylates
CP43 (but not LHCII) shows both redox-dependent
and redox-independent regulation (Vink et al. 2000).
With midpoint redox potentials as low as 0.9 V (primary acceptors of photosystem I), the photosynthetic
electron transport chain generates reductants with potentials far lower than those involved in the mitochondrial
respiratory chain. This and other aspects of the essential
photoelectrochemistry of photosynthesis first evolved in
an anaerobic world, where there was probably little
selective pressure against such low potential components
(Allen 1993). Electron flow from these highly reducing
components is thermodynamically favourable for reduction of oxygen to superoxide (Em7 ¼ 0.33 V). Evolution
358
has led to the integration of signals from such inevitable
side reactions into cellular control mechanisms involving
profound changes in gene function (Allen and Raven
1996, Foyer and Noctor 2000, Noctor et al. 2000).
Because of the potentially high capacity of photosynthesis for the production of superoxide, hydrogen peroxide
and singlet oxygen, the intracellular levels of these
oxidants are tightly buffered and controlled by the
detoxifying antioxidant system, comprising a network
of enzymatic and non-enzymatic components (Noctor
and Foyer 1998, Mittler 2002). Major detoxification
reactions associated with photosynthesis are mediated,
first, by catalase (in the peroxisomes) and, second (in all
compartments), by reductive processes involving the
major redox buffers of plant cells, ascorbate and glutathione pools (Noctor and Foyer 1998).
Two notable, fairly common features of the oxidative
stress response are that (1) the most strongly induced
genes are not necessarily those on the front line of the
antioxidant defence system: genes markedly induced are
those encoding, for example, pathogenesis-related proteins and heat-shock proteins, rather than classical antioxidants; and (2) antioxidant genes that are induced
often tend to encode cytosolic rather than chloroplastic
antioxidative proteins, even in conditions in which the
major stress is predicted to be located in the chloroplast.
For example, cytosolic APX transcripts, as well as the
promoter activity of this nuclear gene, were shown to be
influenced by the redox state of the photosynthetic electron transport chain (Karpinski et al. 1997).
Peroxisomes and reactive oxygen and nitrogen species
Peroxisomes are known to release signals that regulate
nuclear gene expression. Signals arising from peroxisomes regulate photomorphogenesis, plant development
peroxisomal biogenesis, light signalling and stress
responses (Hu et al. 2002). Redox signals are very likely
important in this process since peroxisomes produce
H2O2 at high rates through several reactions, including
b-oxidation of long chain fatty acids and glycollate oxidase. The latter reaction means that during moderate to
high rates of photosynthesis, the peroxisomes of C3
plants are the site of massive light-dependent generation
of H2O2 (Fig. 1). To cope with this, these organelles have
a very high antioxidant capacity, notably including catalase but also APX and other enzymes of the ascorbate/
glutathione system (Jiménez et al. 1997). Catalase is
clearly necessary for photorespiratory H2O2 processing
(Smith et al. 1984, Willekens et al. 1997) and insufficient
activity of this enzyme causes perturbation of cellular
redox state when photorespiration is rapid, notably associated with a marked accumulation of oxidized glutathione. Photorespiration-linked perturbation of the
redox states of both ascorbate and glutathione can
occur transiently in plants with a full complement of
catalase (Noctor et al. 2002), and the glycollate oxidase
reaction could possibly be one way in which signals
Physiol. Plant. 119, 2003
linked to photosynthesis are exported from the chloroplast. Such a mechanism may be important in certain
conditions such as drought, other stresses that decrease
stomatal conductance, or increased temperature. Under
other conditions, such as low temperature, peroxisomal
H2O2 formation will become less important whereas the
probability (although perhaps not the absolute rate) of
mitochondrial and chloroplastic production may tend to
increase in these conditions. It should also be noted that
peroxisomes can generate significant amounts of superoxide from which H2O2 is produced by a peroxisomal
superoxide dismutase (for review, see del Rı́o et al. 2002).
It is possible that peroxisomes are a major site of nitric
oxide (NO) synthesis in plants (Corpas et al. 2001).
There is some evidence to suggest that NO synthase
(NOS), a key enzyme involved in mammalian macrophage action, is conserved in plants (Ninnemann and
Maier 1996, Beligni and Lamattina 2001). An NADPHand Ca21-dependent NOS activity was found in pea
peroxisomes (Barroso et al. 1999). Moreover, a 130-kDa
peroxisomal pea protein was recognized by a polyclonal
antibody raised against 14 residues from the C-terminus
of iNOS (Barroso et al. 1999). Whereas the sequencing
of the complete Arabidopsis genome did not reveal the
presence of putative NOS genes, a complementary
DNA sequence with high homology to a protein NOS
inhibitor, has been described in plants (Jaffrey and
Snyder 1996).
Redox signalling associated with mitochondrial
respiration
Like chloroplasts, mitochondria also originated as
bacterial endosymbionts, and they retain a specialized
genome. Redox signalling as the function of the
mitochondrial genome has wide implications. The ‘free
radical’ and ‘mitochondrial’ theories of ageing are central
tenets to animal and human biology but have not been
explored in plants (Allen 1993). Mitochondria have not
traditionally been regarded as a major source of ROS in
leaves, although it has been known for many years that
reactions associated with complexes I and III produce
superoxide (for review, see Møller 2001). Indeed, various
mitochondrial enzymes, such as aconitase and enzymes
containing lipoic acid, are susceptible to oxidative inactivation. From a whole leaf point of view, however, at
least in C3 plants at moderate to high light intensities,
peroxisomal and chloroplastic H2O2 production may be
up to 30–100 times faster than formation of H2O2 in the
mitochondria (Fig. 1). Interestingly, calculations suggest
that mitochondrial ROS production is not likely to be
greatly different in the light and dark, since total O2
consumption is less affected by light than tricarboxylic
acid cycle activity. However, the probability of superoxide production by the respiratory chain could be
changed on illumination, notably if light affects alternative
oxidase (AOX) capacity (Dutilleul et al. 2003a). This
enzyme influences ROS generation (Maxwell et al. 1999)
Physiol. Plant. 119, 2003
and is involved in the determination of cell survival in
oxidative conditions (Robson and Vanlerberghe 2002,
Vanlerberghe et al. 2002).
It should be noted that the relative rates shown in
Fig. 1 will probably change differentially as a function
of the type of stress applied, and in certain conditions the
mitochondrial contribution may be significant, even in
the light. Even under conditions in which the mitochondria contribute only a fraction of total cellular ROS
production, the mitochondrial oxidative load could be
crucial in influencing and setting the cellular redox-state,
either because of the presence of specific signalling components or because detoxification capacity is relatively
low in comparison with the chloroplast and peroxisome.
Like these other organelles, however, mitochondria
house both enzymic and non-enzymic antioxidants
(Rasmusson and Møller 1990, Jiménez et al. 1997),
including a TRX system (Laloi et al. 2001), and are the
site of ascorbic acid biosynthesis. The final step of
ascorbic acid biosynthesis is catalysed by a galactonog-lactone dehydrogenase located in the inner mitochondrial membrane (Bartoli et al. 2000). Evidence has
recently been obtained that this enzyme is an intrinsic
component of complex I, and that respiratory electron
flow may exert significant control on ascorbate synthesis
(Millar et al. 2003).
Evidence that perturbation of the mitochondria redox
state has important consequences for whole cell redox
homeostasis has been provided by studies on a Nicotiana
sylvestris mutant, CMSII, which lacks functional complex I and has hence lost a major NADH sink. Substantial re-adjustments in antioxidant defence and related
changes in stress tolerance are observed in the mutant
(Dutilleul et al. 2003a). When complex I function is
perturbed, signalling is initiated which resets the antoxidative capacity throughout the cell. This includes
enhanced expression of mitochondrial antioxidants (AOX
and Mn-SOD) and also of chloroplastic Fe-SOD, peroxisomal catalase, and cytosolic APX. Mitochondrial signalling hence acts to lower cellular H2O2 and allows
soluble cellular antioxidants (ascorbate, glutathione) to
retain a high reduction state. This redox re-adjustment is
associated with the inability of the mutant to use its
photosynthetic capacity as efficiently as the wild type
(Dutilleul et al. 2003b), probably due to perturbations
in NAD(P)H shuttling between intracellular compartments (for reviews, see Gardeström et al. 2002, Scheibe
2003). These shuttles represent another example of the
important interactions between chloroplasts and mitochondria, and could be crucial in adjusting the rate of
ROS production in both compartments. Reductant export
from the chloroplast to the mitochondria might act to
lower ROS production in the chloroplast by relieving
electron pressure, while increasing the probability of ROS
formation in the respiratory chain. At the origin of
mitochondrial redox signalling may be changes in the
redox state of ubiquinone or components of the cytochrome bc1 complex, by analogy to the signalling linked
to the chloroplast plastoquinone pool. Such changes could
359
H2O2 concentration is not greatly increased relative to
the wild type but the glutathione pool is massively perturbed (Noctor et al. 2002). Increased availability of
ROS may therefore be sensed by the cell as increased
oxidative flux through key components, rather than (or
as well as) marked increases in ROS concentration
(Fig. 2). This view suggests a dynamic system constructed
to allow acclimatory changes through components of the
antioxidative system that are plugged into signalling networks. It would allow appropriate responses to occur as
a result of increased flux to ROS, even in the absence of
marked changes in ROS concentration. Furthermore,
changes in ROS trigger profound modifications in gene
expression that extend far beyond the antioxidative system (Kovtun et al. 2000, Desikan et al. 2001, Vranova
et al. 2002). This confirms the view that the defence
system comprising pathogen responses, defence against
xenobiotics, stabilizing components, and antioxidants
forms an integrated network with extensive crosstalk
that can be triggered by ROS. Moreover, priming of
different components can be triggered by low ROS
concentrations such that the system responds more
rapidly and/or effectively to subsequent assault (Vranova
et al. 2002). We suggest that some antioxidative components have a dual function of scavenging and signalling
be linked to increased ROS generation through electron
leakage to superoxide.
ROS and redox signal perception and transduction
To date no ROS receptor has been unambiguously identified in plants, and thus a key question is: how is
increased ROS production sensed? One simple possibility
is direct modification of transcription factors with redoxsensitive groups (Tron et al. 2002), but there are very
likely much more complex signal transduction routes.
This must be the case when redox changes in organelles
are signalled to the nucleus. Important sensing components may be found in the antioxidative system itself.
This system is a strong buffer against ROS, maintaining
relatively low oxidant concentrations under most conditions. Although localized increases in ROS can occur in
certain circumstances, such as during the oxidative burst
at the plasmalemma, in many cases redox balance can be
markedly perturbed without large changes in H2O2 concentration. This is, perhaps, not suprising given the
plethora of components capable of scavenging H2O2. In
catalase mutants placed in conditions where the leaf can
no longer cope with photorespiratory H2O2 production,
A Optimal conditions
Detox-scavenging
Photosynthesis
Photorespiration
Respiration
[ROS]
Sensor-scavenging
–
B Stress conditions
Detox-scavenging
+
Photosynthesis
Photorespiration
Respiration
[ROS]
Other defences
+
Acclimatory
pathway
Sensor-scavenging
(Thiol oxidation?
Glutathionylation?)
360
–
OR
Cell death
pathway
Kinase
cascades
Fig. 2. A model for the
perception of increased ROS
production via the antioxidant
system. In optimal conditions
(A), ROS are produced by
many metabolic reactions and
are efficiently removed by
detoxification processes
(‘Detox-scavenging’). Stress
conditions (B) cause increased
production of ROS or
decreased antioxidant activity,
which can cause an increase in
ROS concentration. This could
lead to increased oxidation of
specific ‘sensor-scavenging’
antioxidant components locked
into signal transduction
pathways. Stimulation of
transduction pathways occurs
via kinase cascades and other
second messengers, and leads to
either acclimation (upregulation of ROS
detoxification capacity,
induction of other defences) or
cell death pathways involving
defence withdrawal. The
decisive factors that determine
either acclimatory or cell death
responses are not known, but
could include location of the
initial signal or signal intensity.
Control of cell fate by signal
intensity would be a molecular
application to plants of the
aphorism formulated, more
than a century ago, by the
philosopher Nietszche: That
which does not kill me, makes
me stronger.
Physiol. Plant. 119, 2003
(Fig. 2: ‘sensor-scavenging’ components). These could
perhaps be relatively low in antioxidative capacity comparedtoclassicaldetoxification-scavenging(Fig. 2:‘Detoxscavenging’) components such as catalase or chloroplastic APX.
What could be the nature of such ‘sensor-scavenging’
components)? It is perhaps noteworthy that catalases
and APX are haem-based whereas many other
antioxidant components operate through thiol–disulphide
exchange reactions. As well as the soluble thiol glutathione, the plant cell contains numerous proteins with
redox-active thiol groups, some of which have been
shown to have activity against peroxides. These include
both chloroplastic and cytosolic glutathione peroxidases
(GPX: Eshdat et al. 1997, Mullineaux et al. 1998), chloroplastic and cytosolic PRX (Baier and Dietz 1999, Rouhier
et al. 2001, Horling et al. 2003), and glutaredoxins
(GRX). Specific TRX are also found in several compartments of the photosynthetic cell (Rivera-Madrid et al.
1995). There is considerable heterogeneity within these
families: for PRX, there are monomeric and dimeric
enzymes, and differences in the number of Cys involved
in catalysis. Similarly, several sequences predicted to
encode TRX-like proteins and both dithiol and monothiol GRX-like proteins (Vlamis-Gardikas and Holmgren
2002) are found in the Arabidopsis genome. Although
the exact roles of most of these plant thiol proteins
remain to be elucidated, it is clear there may be considerable divergence of function within each class.
In mammals, where TRX exists as mitochondrial
(TRX2) and cytosolic/nuclear (TRX1) forms, expression
is influenced by an ARE (antioxidant response element)
cis-acting factor, and TRX1 mediates numerous defence
processes, including Ref-1 activity and the nuclear versus
cytosolic localization of the transcription factor NF-kB
(Vlamis-Gardikas and Holmgren 2002). Recently, it has
been shown in yeast that the redox transduction sensor,
YAP-1, interacts in a complex fashion with both TRX
and non-selenium (i.e. plant-type) GPX (Delauney et al.
2002). YAP-1 is a basic zipper-type transcription factor
that induces several genes in response to peroxides. Peroxides enhance the nuclear accumulation of YAP-1 by
oxidizing two Cys residues to form an intramolecular
disulphide bond that appears to act to trap YAP-1 in
the nucleus, thereby increasing its activity (Kuge et al.
1997). Oxidation of YAP-1 is not mediated directly,
however, but occurs via H2O2 reduction by a GPX-like
protein, which is then reduced by YAP-1 (Delauney et al.
2002). Re-reduction of YAP-1 may occur by a TRXdependent pathway (Delauney et al. 2002). Although
the Arabidopsis genome does not appear to contain
sequences homologous to YAP-1, there may well be
functionally similar elements in the initial perception of
changes in redox state in plants. PRX are often alternatively termed TRX peroxidase and chloroplastic PRX
purified from Chlamydomonas has been shown to reduce
peroxides using reductant from TRX (Goyer et al. 2002).
This enzyme system is therefore closely linked to the photosynthetic electron transport chain in vivo, probably via a
Physiol. Plant. 119, 2003
novel, specific chloroplastic TRX isoform (Collin et al.
2003). A PRX localized in poplar phloem can function
with either the TRX h/NADPH-TRX reductase or GRX/
glutathione/GR systems (Rouhier et al. 2001). It is possible
that the primary role of at least some of these thiol proteins, particularly those with relatively low capacity, is not
to detoxify peroxides but to sense their increased production, that is, their most important function may be as signal
or signal-scavenging components (Fig. 2).
Net oxidation of the glutathione pool, accompanied
by increased total glutathione, is a clearly established
response to many stresses or to insufficient detoxification
capacity (Smith et al. 1984, Sen Gupta et al. 1991,
Willekens et al. 1997, Noctor et al. 2002). A mechanism
important in sensing this redox perturbation may be
protein glutathionylation, in which glutathione forms a
mixed disulphide with a target protein. In yeast and
animals, glutathionylation has been shown to modify
the activity of enzymes and transcription factors and is
considered likely to play an important role in redox
signalling and protection of protein structure and function (Klatt and Lamas 2000). For example, gluthathionylation of aldolase and triose phosphate isomerase has
recently been reported in Arabidopsis leaves (Ito et al.
2003). Spontaneous formation of mixed disulphides may
require decreases in GSH/GSSG that are not thought to
be physiologically relevant, at least in most mammalian
cells, but in the absence of marked accumulation of GSSG
the reaction can be catalysed by GRX (Starke et al. 2003).
Reversal of glutathionylation may be carried out
by dithiol or monothiol GRX, as well as the dithiol protein,
TRX. It is interesting to note that these components belong
to a large super-family of proteins, and that proteins related
to classical TRX, but with a monocysteinic active site
motif, also exist in plants. Considerable work will be
required to elucidate the functions of many of these proteins. It is possible that whereas only the dithiol enzymes
have activity against protein disulphide bonds, the monothiol GRX may be the most important in deglutathionylating mixed disulphides to protein-SH and GSH (Shenton
et al. 2002, Vlamis-Gardikas and Holmgren 2002).
Another important group of thiol proteins may be
certain subclasses of the GST super-family that are active
in reducing peroxides or dehydroascorbate (DHA), or in
catalysing thiol transferase (i.e. GRX) activity (Bartling
et al. 1993, Dixon et al. 2002). Some GSTs are strongly
induced by oxidative stress, including that linked to the
pathogen response (Conklin and Last 1995, Desikan et al.
2001, Dixon et al. 2002). Until recently considered as
exclusively cytosolic enzymes, GSTs form a large gene
family in Arabidopsis, but the physiological functions of
many of these genes remain unclear. Lately, it has been
shown that in two subclasses of the GST family found in
Arabidopsis, the classical GST active site Ser is replaced
by Cys (Dixon et al. 2002). This confers both DHA
reductase and GRX activity on the first class, and
DHA reductase activity on the second: in each class,
gene sequences predicted at least one chloroplastic and
one cytosolic product (Dixon et al. 2002).
361
Integration of redox signalling and plant development:
interactions between ROS and phytohormones
While redox sensing in plants may have some similarities
with that observed in yeast, downstream signalling is
probably more intricate, because the photosynthetic,
multicellular nature of plants necessitates integration of
a complex array of internal and external signals during
development. MAP kinase cascades are implicated in the
H2O2 response in plants (Kovtun et al. 2000). In signalling linked to hormones such as ethylene and cytokinins,
such cascades are frequently initiated by specific
two-componentphosphorelayreceptors(Schaller2000,Inoue
et al. 2001), and it may be that analogous redox-sensitive
receptors are important in ROS signal sensing. Available
data point to both upstream and downstream interactions between ROS production and the action of
hormones such as abscissic acid (ABA) and ethylene (Pei
et al. 2000, Desikan et al. 2001, Moeder et al. 2002). Leaf
ascorbate content has recently been shown to impact on
ABA content and signalling (Pastori et al. 2003). Ascorbate deficiency in the Arabidopsis thaliana vtc1 mutant,
associated with slow growth and late flowering, led to the
differential expression of 171 genes. Many of these were
genes involved in plant defence but transcript changes also
indicated that growth and development are constrained in
vtc1 by modulation of the balance between ABA and
gibberellic acid (GA) signalling (Pastori et al. 2003). Incubating vtc1 leaf discs in ascorbate can reverse key features
of the molecular signature of ascorbate deficiency. Feeding ascorbate modified the abundance of 495 transcripts
including genes involved in plant defence and photosynthetic metabolism, notably those encoding TRX-regulated
chloroplast enzymes (Kiddle et al. 2003).
Conclusions and perspectives
Plants have created the aerobic world in which we live
and use redox reactions and signals, particularly those
involving oxygen, in all aspects of their biology. There is
no doubt that oxygen is potentially toxic and that all
aerobic life forms survive by virtue of efficient antioxidant systems. It is therefore not surprising that the
amounts of major antioxidants such as ascorbate are
sensed and exert control over plant growth and development. Oxygen is a very useful substrate for energy
exchange reactions and has hence been incorporated into
both photosynthetic and respiratory energy exchange
reactions. The power of its radical (superoxide, hydroxyl
radical) and non-radical (hydrogen peroxide) derivatives
can be effectively harnessed (because ROS are relatively
short-lived) to convey redox information or unleashed,
when antioxidant defence is withdrawn, to trigger cell
death. These signals are incorporated into the complex
redox network that involves the intrinsic electron carriers
(plastoquinone, ubiquinone) and electron acceptors (ferredoxin, TRX). It is crucial to note that molecular oxygen
is a natural oxidant of plastoquinone, ferredoxin and
TRX, and that such auto-oxidation reactions produce
362
superoxide. Moreover, there are numerous interactions
between redox and hormonal controls. These situate
ROS and antioxidants at the heart of the fine control of
plant development and acclimation to external conditions,
and suggest that elucidating the details of the signalling
networks will be a challenging and fascinating task.
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