Chloroplasts as source and target of cellular

Journal of Experimental Botany, Vol. 56, No. 416, pp. 1449–1462, June 2005
doi:10.1093/jxb/eri161 Advance Access publication 29 April, 2005
FOCUS PAPER
Chloroplasts as source and target of cellular redox
regulation: a discussion on chloroplast redox
signals in the context of plant physiology
Margarete Baier* and Karl-Josef Dietz
Biochemistry and Physiology of Plants, University of Bielefeld, D-33501 Bielefeld, Germany
Received 28 January 2005; Accepted 15 March 2005
Abstract
During the evolution of plants, chloroplasts have lost
the exclusive genetic control over redox regulation and
antioxidant gene expression. Together with many other
genes, all genes encoding antioxidant enzymes and
enzymes involved in the biosynthesis of low molecular
weight antioxidants were transferred to the nucleus.
On the other hand, photosynthesis bears a high risk for
photo-oxidative damage. Concomitantly, an intricate
network for mutual regulation by anthero- and retrograde signals has emerged to co-ordinate the activities
of the different genetic and metabolic compartments. A
major focus of recent research in chloroplast regulation addressed the mechanisms of redox sensing and
signal transmission, the identification of regulatory
targets, and the understanding of adaptation mechanisms. In addition to redox signals communicated
through signalling cascades also used in pathogen
and wounding responses, specific chloroplast signals
control nuclear gene expression. Signalling pathways
are triggered by the redox state of the plastoquinone
pool, the thioredoxin system, and the acceptor availability at photosystem I, in addition to control by
oxolipins, tetrapyrroles, carbohydrates, and abscisic
acid. The signalling function is discussed in the context of regulatory circuitries that control the expression
of antioxidant enzymes and redox modulators, demonstrating the principal role of chloroplasts as the source
and target of redox regulation.
Key words: Abscisic acid, antioxidants, chloroplast, gene
expression, oxolipin, peroxiredoxin, photosynthesis, redox
regulation, signalling, stress.
Introduction
In plants, photosynthesis generates redox intermediates
with extraordinarily negative redox potentials. Light-driven
electron transport transfers electrons from the acceptor site
of photosystem I (Em < ÿ900 mV) to various acceptors
including oxygen (Em = 815 mV; Blankenship, 2002). The
redox intermediates cover an exceptionally wide range of
mid-point redox potentials (Dietz, 2003) with a significant
risk for electron transfer to oxygen and other appropriate
targets. Among the best known examples for chloroplast
redox chemistry is the direct electron transfer from reduced
ferredoxin to O2 in the so-called Mehler reaction (Mehler,
1951). The superoxide radicals formed can be quickly
converted into H2O2 and highly reactive hydroxyl radicals
(HOc) (Elstner, 1990). Together with reactive oxygen
species (ROS) generated by other sources, they are a continuous threat to cellular constituents for uncontrolled
oxidation.
In the context of (i) the physiologically bivalent oxygen
chemistry, (ii) the demand for reductive power, and (iii) the
peril of excess photosynthetic electron pressure, chloroplasts are prone to oxidative damage like no other organelle
(Foyer et al., 1997). Consequently, photosynthetic organisms have evolved defence mechanisms to control the redox
poise of the electron transport chain and the redox environment of the stroma. They range from the suppression of
* To whom correspondence should be addressed. Fax: +49 (0)521 106 6039. E-mail: [email protected]
Abbreviations: 2CPA, 2-Cys peroxiredoxin A; ABA, abscisic acid; DBMIB, 3-methyl-6-isopropyl-p-benzoquinone; DCMU, 3-(39,49-dichlorophenyl-)1,1dimethyl urea; DOX, fatty acid dioxygenase; Em, mid-point potential; LOX, lipoxygenase; MAPK(K)(K), mitogen activated protein kinase (kinase) (kinase);
NDH, NAD(P)H dehydrogenase; PET, photosynthetic electron transport; PQ, plastoquinone; Prx, peroxiredoxin; ROS, reactive oxygen species; Rubisco,
ribulose-1,5-bisphosphate carboxylase oxygenase.
ª The Author [2005]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For Permissions, please e-mail: [email protected]
1450 Baier and Dietz
ROS generation and avoidance of uncontrolled oxidation of
essential biomolecules by accumulating high concentrations of low-molecular weight antioxidants to repair mechanisms by reduction and de novo synthesis of damaged
molecules. In the illuminated chloroplast, the reduction
energy for the regeneration of oxidized metabolites is
mainly taken from the photosynthetic electron transport
(PET). Depending on the photo-oxidative strain, up to
almost 100% of the photosynthetically transported electrons can be diverted into the antioxidant defence system
(Asada, 2000). In the dark, when the strong reductive
power of photosynthesis is missing, the redox environment
of chloroplasts probably adjusts to redox potentials similar
to those measured in the cytoplasm of heterotrophic cells
(i.e. below ÿ300 mV to approximately ÿ240 mV; Dietz,
2003). Under these conditions, chloroplasts stabilize their
redox poise by metabolization of starch and import of
reduction energy.
Studies with various transgenic plant lines and mutants
demonstrated the importance of a high antioxidant capacity as realized by low-molecular weight antioxidants
(Pastori et al., 2003; Ball et al., 2004) and antioxidant
enzymes (Willekens et al., 1997; Baier et al., 2000;
Davletova et al., 2005). The antioxidant defence system responds to redox imbalances. The pool size of low molecular weight antioxidants and the expression of chloroplast
antioxidant enzymes increases if the photo-oxidative strain
on the system is high (Foyer et al., 1997). Interestingly,
oxidizing conditions correlate with a high reduction state,
since, as outlined above, excess electrons are transferred
to O2 that, in turn, abstract electrons from organic targets.
This apparent contradiction (‘high reducing activity
results in oxidizing conditions’) will be important for
understanding redox regulation, as for example in the
peroxiredoxin function, in the context of photosynthesis
(see below). However, all chloroplast antioxidant enzymes
and all enzymes involved in the biosynthesis of lowmolecular-weight antioxidants are nuclear encoded. The
spatial separation of expression and function demands for
signal transduction over the chloroplast envelope. Deviations from regular redox homeostasis can be sensed in the
chloroplast and transmitted to the nucleus by retrograde
signalling cascades. Alternatively, redox imbalances in the
chloroplast could be transmitted into the cytoplasm by
metabolic coupling (Fig. 1). The sensor then resides in
the cytoplasm. Transmission of redox signals suffers
from the drawback that cytoplasmic redox homeostasis
and antioxidant defence will strongly damp the spreading
signal.
Another terminology to be clarified is the distinction of
signalling and regulation. Both terms are used with a broad
meaning here. Regulation describes any adjustment of
activity, i.e. of enzymes or transcription factors, while
signalling refers to any transport of information from one
site to another via a signalling molecule that, by itself,
Fig. 1. The cytosolic antioxidant system shields the nucleus from chloroplast ROS signals. Photosynthetic ROS signals and redox imbalances are
buffered by cytosolic antioxidants. Whether they reach the nucleus
depends on the rates of ROS-formation and the strength of the cytosolic
antioxidant system. In contrast, a non-redox active second messenger can
pass the cytosol without loss of function.
may have additional functions, for example, as a metabolic
intermediate.
Redox coupling
All redox active compounds together define the cellular
redox poise of a cell (Schafer and Buettner, 2001). In
addition to the redox energetics defined by the mid-point
potentials and the concentrations of the various antioxidants, the redox state of a particular compound is under the
control of kinetic constraints defining the reaction constants.
Enzymes lower the kinetic barriers and couple redox pairs.
Recycling of oxidized intermediates, as well as regeneration
of the reductants, affect the redox state of specific redox
pairs (Dietz, 2003). Different drainage rates of electrons
from antioxidants and weak enzymatic linkages can uncouple the redox states of individual components of the
antioxidant network, as has been observed for ascorbate and
glutathione. While specific oxidation of the glutathione pool
took place in catalase-deficient barley (Willekens et al.,
1997), reduced 2-Cys peroxiredoxin levels led preferentially to the oxidation of the ascorbate pool in Arabidopsis
thaliana (Baier et al., 2000). The favoured oxidation of
glutathione in the catalase-lines is proposed to be caused by
higher cytosolic dehydroascorbate reductase activity rather
than glutathione reductase activity, while the redox shift in
the ascorbate pool in the peroxiredoxin antisense plants
might be caused by insufficient dehydroascorbate reductase
activity in the chloroplasts (Noctor et al., 2000). For cellular
redox homeostasis and redox metabolism, the nature of
a particular antioxidant employed in a specific detoxification reaction and, within limits, the relative redox state of an
Chloroplast redox regulation
individual antioxidant may be of minor importance. However, deviations from redox normality can serve in signal
generation and signal transmission.
Defining redox signals in the context of
photosynthesis
The nature of the redox signals perceived, the sensory
systems, and the classification of the respective responses
have received increasing attention in recent years. In plant
biology special focus has been given to redox signal
transduction in chloroplasts as well as between chloroplasts and the nucleus for experimental and thematic
reasons. (i) The metabolic state of chloroplast metabolism
can easily be manipulated by altering exogenous parameters such as light, CO2, and temperature. (ii) Tools such
as chlorophyll a fluorescence-based technology to estimate
photosynthetic efficiency and redox state, methods at
virtually all levels of molecular biology and biochemistry,
and a vast accumulated body of knowledge on structure,
function, regulation, and assembly facilitate interpretation
of the results. (iii) Photosynthesis exerts a strong impact
on the cellular redox signature and nuclear gene expression and regulates the photosynthetic capacity during longterm adaptation (Dietz, 2003). However, the hypothesis,
on retrograde redox signalling originating inside chloroplasts, is generally accepted and despite these systematic
advantages, the precise nature of the signals, their specificity and interaction are only recently becoming tangible.
Theoretical considerations and experimental data have
produced a long list of potential signals, of which a selection
is discussed here in the context of the regulation of genes
involved in the control of the cellular redox poise. Due to
the complexity of the possible chemical nature and origin of
the signals, defining redox signals depends on the line of
vision and the intention. For example, Dietz (2003) grouped
redox signals based on their origin and mode of action in
signal transmission. According to his definition, type-I
signals derive specifically from single pathways, while
type-II signals integrate redox information from various
pathways; type-III redox signals indicate more extreme
redox imbalances and their transmission depends on crosstalk with other signalling cascades. Other definitions for
redox signals are based on the threshold of induction relative
to photosynthetic electron pressure (Pfannschmidt et al.,
2001a) or on their putative initiation sites (Pfannschmidt
et al., 2003). For chloroplast-to-nucleus signalling, which
depends on passing the chloroplast envelope, a classification
based on the chemical nature of the signalling compound
leaving the chloroplast has been proposed (Baier and Dietz,
1998). Based on this chemical classification, a concept is
followed here in which signals transmitted by redox shifts in
cellular redox components or by ROS are distinguished
from signals transmitted by second messengers synthesized
inside chloroplasts (Fig. 1).
1451
Sensing the cellular redox poise
Compelling experimental evidence for redox regulation of
nuclear gene expression is available for redox signalling
induced by the application of ROS, ROS-inducing stressors, low availability of antioxidants, and by antioxidant
feeding, respectively. The common feature of all these
treatments is that the cytosolic redox environment specifically or generally is shifted to a more oxidized or reduced
state. In the context of signal transmission, special attention
has been given to H2O2 (Desikan et al., 2001; Mittler et al.,
2004; Vandenabeele et al., 2004). Alternatively, monitoring the cellular redox environment by sensing the redox
state of certain metabolites, for example, glutathione and
ascorbate, has been postulated (Foyer et al., 1997; Dietz,
2003; Pastori et al., 2003; Ball et al., 2004). Both types of
metabolites, ROS and low-molecular-weight antioxidants,
closely interfere. Consequently, in most experiments it is
hardly possible to distinguish between signalling that is
possibly originating from H2O2 and that from shifts in the
redox poise of low-molecular-weight antioxidants. Therefore, they are discussed here together.
Recently cDNA array hybridization experiments were
performed and indicate a strong regulatory function of
redox signals on nuclear gene expression. For example,
Desikan et al. (2001) analysed the response of Arabidopsis
thaliana to H2O2 application and Mahalingham et al.
(2003) to ozone. Pastori et al. (2003) investigated the regulation of transcript amounts in the low-ascorbate mutant
vtc1 and Vandenabeele et al. (2004) that in a catalasedeficient tobacco line, as well as Davletova et al. (2005)
that of a knock-out mutant of cytosolic ascorbate peroxidase APx1, and Ball et al. (2004) determined the transcriptional response of the allelic glutathione biosynthetic
mutants rax1-1 and cad2-1. Typical target genes with
altered transcript accumulation upon treatment or in the
mutants are those for PR proteins, e.g. PR1 (At2g14610),
chitinase (At2g43570), and PAL (encoding phenylalanine
ammonium lyase; At3g53260; At5g04230), and antioxidant enzymes as peroxidases (e.g. At4g11290 and
At4g21960), dehydroascorbate reductase (At1g19570)
and CuZn-superoxide dismutase (At5g18100). The sets of
target genes widely overlap with the transcripts induced by
pathogens and wounding (Mahalingam et al., 2003;
Cheong et al., 2002).
The transcription factors involved in these responses were
tentatively identified either by being up-regulated at the
transcriptional level (Mahalingam et al., 2003; Pastori
et al., 2003; Ball et al., 2004; Davletova et al., 2005) or
through the bioinformatic comparison of promoters for
stress-induced transcripts (Chen et al., 2002). Candidate
transcription factors are WRKY (W-box: TTGACY;
Euglem et al., 2000), WRKY-like (BBWGACYT; Chen
et al., 2002), SA (ACGTCA; Lebel et al., 1998), b-ZIP of
the TGA1-type (TGACG; Schindler et al., 1992), GBF-type
1452 Baier and Dietz
(CACGTG; Schindler et al., 1992) and ABRE-type
(BACGTGKM; Shinozaki and Yamaguchi-Shinozaki,
2000), Myb (AtMyb1: MTCCWACC; AtMyb2: TAACSGTT; AtMyb3: TAACTAAC; AtMyb4: AMCWAMC;
Martin and Paz-Ares, 1997; Rushton and Somssich, 1998),
and AP2-like transcription factors (GCCGCC for GCC-box
binding AP2s or DRCCGACNW for DRE-binding AP2s;
Shinozaki and Yamaguchi-Shinozaki, 2000).
In response to the many stressors inducing shifts in the
cellular redox poise, for example, wounding, pathogens,
ozone, UV-B, and cadmium application, mitogen activated
protein kinases (MAPK) play a critical role in signal
transduction (Cheong et al., 2002; Holley et al., 2003;
Yeh et al., 2004). Specifically, MPK3, MPK4, and MPK6
are activated by various abiotic stresses (Ichimura et al.,
2000; Kovtun et al., 2000) making them candidates for
signal transduction in redox regulated stress signalling.
Upstream in signal transduction, the MAPKs, MPK3 and
MPK6, which are activated by the MAPKKs, MKK4 and
MKK5 (Asai et al., 2002) and the MAPKKK ANP1
(Kovtun et al., 2000), interact with the nucleotide diphosphate kinase AtNDPK2 in Arabidopsis thaliana. By stimulation of the phosphorylation activity of MPK3 AtNDPK2
provides enhanced tolerance to multiple stress responses
(Moon et al., 2003). The MAPK signalling cascades, which
resemble animal redox signal transduction pathways
(Halliwell and Gutteridge, 1999), are subjected to an
additional redox modulation by redox regulation of antagonistic phosphatase activities (Mittler et al., 2004).
In addition to MAPK signalling, thiol-disulphide transitions can control gene expression in response to ROS
accumulation and changes in the cellular thiol homeostasis. By switching of the DNA-binding activity or the
nuclear-cytoplasmic distribution of transcription factors, gene
activity can directly be redox regulated (Sun and Oberley,
1996). Indications for target thiols are the cysteine
residues in the C2H2-domains of WRKYs (Maeo et al.,
2001) and Cys-260 and Cys-266 in TGA1 whose oxidation
prevents binding of the transcription activator protein
NPR1 (NON-REPRESSOR OF PR GENES) (Després
et al., 2003).
However, in chloroplast-to-nucleus signalling, a redox
signalling pathway triggered by redox imbalances in the
cytosol may only occur under severe oxidative stress.
Under physiological conditions, the availability of reduction energy in conjunction with antioxidant enzymes will
maintain the reducing state of the cytosol and quench ROS
signals (Fig. 1). The role of chloroplast metabolism,
particularly of photosynthesis, in ROS and antioxidantdependent redox regulation has been most intensely studied
for the transcriptional control of the cytosolic ascorbate
peroxidase apx2. In excess light, the apx2 promoter is
strongly stimulated (Karpinski et al., 1997), presumably by
the light-induced accumulation of H2O2 (Chang et al.,
2004) and/or a decrease in the reduction state of leaf
glutathione (Karpinski et al., 1997; Ball et al., 2004).
Consistently, inhibition of PET by DCMU (Karpinski
et al., 1997) and (over-) expression of catalase or ascorbate
peroxidase in chloroplasts (Yabuta et al., 2004) suppress
the high-light-dependent induction of apx2. Constitutive
expression of apx2 in the rax1-1 mutant, which is affected
in chloroplast glutathione biosynthesis by decreased cglutamyl cysteine synthetase activity (Ball et al., 2004),
also points at signal initiation depending on oxidative
stimuli. Transcripts for cytosolic APx2 accumulated in
parallel to a decrease in the photochemical quench (qP),
prior to the accumulation of H2O2, and responded differentially to DCMU and DBMIB, which block PET before
and after the PQ pool, respectively. Therefore, Yabuta et al.
(2004) reinstated the hypothesis, originally presented by
Karpinski et al. (1997), that a redox change in PET,
presumably the redox state of the plastoquinone pool,
controls nuclear expression of cytosolic APx2.
Apx2 is regulated by a heat shock factor, namely HSF3
(Panchuk et al., 2002). In the regulation of apx1, which is
also H2O2-responsive, the heat-shock factor HSF21 is
involved in H2O2-sensing (Davletova et al., 2005).
HSF21 transmits the redox signal to the zinc-finger
protein Zat12 (Rizhsky et al., 2004), whose expression is
under the control of HSF21 (Davletova et al., 2005).
Results from apx1 knock-out mutants of Arabidopsis
thaliana suggests that cytosolic ascorbate peroxidase activity is involved in signal transmission in excess light,
including ROS-based signal transmission between the
chloroplasts and the nucleus (Davletova et al., 2005). The
sensitivity of ascorbate peroxidases to inhibition by ROS
(Miyake and Asada, 1996), may facilitate signal transmission by micro-bursts.
For the regulation of nuclear-encoded chloroplast antioxidant enzymes, transcriptome analysis (Kimura et al.,
2003; Davletova et al., 2005), the analysis of transcript
amount for the regulation of chloroplast ascorbate peroxidase (Yoshimura et al., 2000), the chloroplast peroxiredoxins (Baier and Dietz, 1997; Horling et al., 2003),
chloroplast superoxide dismutases (csd2, fsd1; Kliebenstein
et al., 1998), and glutathione peroxidase gpx1 (Milla et al.,
2003) revealed a lower sensitivity of gene expression to
shifts in the cytosolic redox poise compared with nonplastidic antioxidant enzymes. However, in 2-Cys peroxiredoxin antisense lines of Arabidopsis thaliana, in which
a specific component of the chloroplast enzymatic redox
defence was suppressed, the transcripts of chloroplast
monodehydroascorbate reductase and stromal and thylakoid ascorbate peroxidase were selectively induced (Baier
et al., 2000). Loss of 2-Cys peroxiredoxin function led to
slight photoinhibition, damage of the photosynthetic membrane, and oxidation of the ascorbate pool, suggesting
photo-oxidative stress (Baier and Dietz, 1999b). The fact
that three transcripts for chloroplast antioxidants accumulated, while the transcript levels for various other antioxidant
Chloroplast redox regulation
enzymes did not respond, indicates chloroplast-specific
signals triggering nuclear expression (Baier et al., 2000).
Chloroplast-to-nucleus redox signals for
transmission of moderate redox imbalances
Efficient transmission of a signal depends on a low threshold concentration. Accumulation of the signal, in turn, is
controlled by its stability within the metabolic network.
Therefore, messengers that are metabolically more inert and
cannot or can only slowly be inactivated are more efficient
than redox compounds such as ROS and oxidized antioxidants that are decomposed or reduced, respectively, during
diffusion through the cell. In respect of chloroplast-tonucleus signalling, several putative signals have been
suggested, of which some will be discussed here.
Tetrapyrrole signals
Indications for tetrapyrrole signals come from the analysis
of cab gene expression during de-etiolation of Arabidopsis
seedlings (Susek et al., 1993). The arrest of chloroplast
development by a norflurazone-mediated block of carotenoid biosynthesis suppressed the expression of various
nuclear-encoded chloroplast proteins, for example, Lhcb1,
PsbR, RbcS, PetH, and PetE, during early seedling development (Harpster et al., 1984; Mayfield and Taylor,
1984; Bolle et al., 1994; Gray et al., 1995). Based on these
observations, retrograde chloroplast signals were hypothesized for the control of nuclear transcription (Taylor, 1989).
A first insight into signalling was provided by Susek et al.
(1993), who isolated Arabidopsis mutants (gun), that
express cab3, encoding Lhcb1-2, although chloroplast
development had been arrested by norflurazone. Mapping
of the mutations showed defects in haem oxidase (gun2),
phytochromobilin synthase (gun3), a regulator of Mgchelatase (gun4), and the H-subunit of Mg-chelatase
(gun5) (Mochizoki et al., 2001; Larkin et al., 2003; Strand
et al., 2003) indicating a role of tetrapyrrole biosynthesis in
the regulation of nuclear transcription (Strand et al., 2003).
Either Mg-protoporphyrin-IX, haem or a haem precursor
were assumed to be released from chloroplasts and to
modify nuclear gene expression by binding to a regulatory
protein, which interacts with the CUF1-element found in
several promoters of 70 genes mis-regulated in gun2 and
gun5 (Strand et al., 2003; Strand, 2004).
In higher plants, the pathways of chlorophyll and haem
biosynthesis are tightly regulated at an early step. Haem
triggers feed-back inhibition of Glu-tRNA reductase, which
catalyses biosynthesis of the tetrapyrrole precursor daminolevulinic acid (ALA) (Beale, 1999). While haem
binds to the N-terminus of the enzyme (Vothknecht et al.,
1998), FLU, which is a negative regulator of chlorophyll
biosynthesis (Meskauskien et al., 2001), regulates GlutRNA reductase at the C-terminus (Goslings et al., 2004).
1453
Characterization of the mutant ulf3, which is allelic to gun2
(Susek et al., 1993), demonstrated that tetrapyrrole biosynthesis is concurrently regulated by FLU mediating the
feedback from the Mg2+ branch and ulf3/gun2 controlling
the haem branch (Goslings et al., 2004), which makes
tetrapyrroles unlikely to accumulate in mature tissues. In
addition, Keetman et al. (2002) showed, in tobacco
coproporphyrinogen oxidase antisense lines, which accumulate protoporphyrin-IX, that imbalances in tetrapyrrole
biosynthesis primarily lead to modulation of gene expression by photosensitization of the pigments. Redox signals,
for example, H2O2 accumulation or shifts in the redox state
of low-molecular-weight antioxidants, may be involved in
the suppression of nuclear gene expression in norflurazonetreated seedlings, although Strand et al. (2003) excluded
severe differences in the steady-state levels of superoxide
for the gun mutants by semi-quantitative NBT-staining. In
mature leaves, expression of cab3, which was used as
a target gene in the gun-screen, is regulated by photosynthetic electron transport (Sullivan and Gray, 2002), presumably by the acceptor availability of photosystem I
(Pursiheimo et al., 2001). Photo-damaged tetrapyrroles
may regulate nuclear gene expression, as for example,
photo-oxidized haem controls the capping of catalase
mRNA in rye (Schmidt et al., 2002).
Oxolipin signals
Besides oxidatively damaged tetrapyrroles, oxolipins are
another type of putative redox-related signals in chloroplastdependent redox regulation. In pathogen response, for
example, they modulate oxidative bursts (Rao et al., 2000).
Their biosynthesis initiates from alkyl hydroperoxides,
which are formed preferentially under unfavourable conditions by oxidation of unsaturated fatty acids either
mediated by ROS (Blée and Joyard, 1996), lipoxygenase
(LOX) (Feussner and Wasternack, 2002) or fatty acid
dioxygenases (DOX) (de Leon et al., 2002). Detailed
time-resolved mass spectrometric analysis of lipids and
lipid hydroperoxides (Montillet et al., 2004) revealed early
activation of the 13-LOX pathway in response to various
kinds of stresses. By contrast, ROS-mediated peroxidation,
which is stimulated by excess excitation energy, appears to
be a late process (Montillet et al., 2004) when the antioxidant defence is close to oxidative collapse. Various plant
signalling molecules are synthesized from alkyl hydroperoxides (Blée and Joyard, 1996). Jasmonates, which are
a group of 12-carbon fatty acid cyclopentanones and dinoroxo-phytodienoic acids, and 2(R)-hydroperoxide fatty
acids, and are well known from pathogen and wounding
responses, protect plant cells from oxidative stress and cell
death (Farmer et al., 1998; Mauch et al., 2001; Hamberg
et al., 2003).
Inside the chloroplast, accumulation of lipid peroxides is
suppressed by glutathione peroxidases and peroxiredoxins.
1454 Baier and Dietz
Both enzymes are haem-free peroxidases reducing alkyl
hydroperoxides by a thiol-based reaction mechanism (Baier
and Dietz, 1999a). The genome of Arabidopsis thaliana
contains two open reading frames for chloroplast glutathione peroxidases (gpx1 and gpx7), of which only gpx1 is
expressed (Milla et al., 2003), and four open reading frames
for chloroplast peroxiredoxins (Horling et al., 2003).
Peroxiredoxins and gpx1 are induced by H2O2 and butylhydroperoxide (Horling et al., 2003; Avsian-Kretchmer
et al., 2004) indicating that their expression possibly
antagonizes oxolipin signal formation. However, expression of gpx1 and 2CPA, which are the only isogenes for
which the analysis has been performed so far, are not
responsive to jasmonates or salicylates (Milla et al., 2003;
Baier et al., 2004) suggesting primary control of oxolipin
biosynthesis by the relative rates of fatty acid peroxidation.
Peroxide formation and reduction may be further uncoupled
due to the sensitivity of the active site cysteine residues to
over-oxidation. 2-Cys Prx have been suggested to function as flood gates that normally keep peroxides at a low
level (Wood et al., 2003; König et al., 2003). Following
a sudden increase in peroxides they are over-oxidized and
inactivated. Subsequently, the oxolipin signal can spread
freely as shown for mammalian cells (Wood et al., 2003).
Glutathione peroxidases, which show only low activities
in plant cells, and the ascorbate peroxidases, which are
highly specific for H2O2 and sensitive to inactivation by
low ascorbate availability, are very likely not able to
compensate for decreased Prx activity. Plant 2-Cys Prx is
efficiently inactivated especially by bulky peroxides, like
lipid peroxides (König et al., 2003). Therefore, with the
accumulation of alkyl hydroperoxides, oxolipin biosynthesis may get increasingly dependent on LOX-, DOX-,
and ROS-stimulation.
In recent years various mutants with decreased sensitivity to jasmonates (and salicylates) and high sensitivity to
ROS have been isolated, for example, the jin (Berger et al.,
1996), jar (Staswick et al., 2002), coi1 (Xie et al., 1998),
npr1 (Scott et al., 2004), rcd1 (Ahlfors et al., 2004), and oji
mutants (Kanna et al., 2003). Although primarily investigated in relation to the wounding and pathogen response,
the signal transduction elements identified could also be
involved in any other type of oxolipin signalling, such as in
the chloroplast-to-nucleus signalling discussed here. The
first components of jasmonate signal transduction have
been cloned: Jin1, which is essential for discrimination
between different jasmonate-regulated defence responses,
encodes the transcription factor AtMyc2 (Lorenzo et al.,
2004), the F-box protein COI1 with 16 leucine rich motifs
(Xie et al., 1998), and the WWE-protein RCD1 (Ahlfors
et al., 2004). Recent cloning of JAR1, which encodes
a jasmonate amino acid synthetase, showed that jasmonates
are activated by conjugation to isoleucine (Staswick and
Tiryaki, 2004) which is another chloroplast-derived
metabolite.
Photosynthetically controlled signals
The redox state of the plastoquinone pool: Efficient regulation of gene expression in relation to photosynthesis should
directly respond to photosynthetic activity. In recent years,
photosynthetic control of both nuclear as well as plastid
gene expression has been linked to the redox state of the
plastoquinone (PQ) pool which regulates expression of, for
instance, petE2 (Pfannschmidt et al., 2001b), encoding a
plastocyanin, in sugar-starved cells (Oswald et al., 2001)
and under low light conditions (Pfannschmidt et al.,
2001b). A small pool of 7–10 PQ molecules per photosystem II mediates electron transfer between photosystem II
and the cytochrome b6 f-complex, making plastoquinol
diffusion the rate limiting step (Haehnel et al., 1984). The
relative activities of photosystem II as electron input and
photosystem I as drainage, cyclic electron transport and
chlororespiration adjust the redox state of PQ (Allen, 1992;
Heber, 2002). Depending on the PQ redox state presumably by binding of plastoquinol to the cytochrome b6 fcomplex (Zito et al., 1999), the kinase TAK1 is activated
and initiates processes like state transition (Snyders and
Kohorn, 2001). Whether this kinase also transmits other
kinds of PQ-dependent responses, for example, in the
regulation of psaAB transcription (Pfannschmidt et al.,
1999) and nuclear expression of petE2, or whether PQ
triggers several independent signal transduction cascades in
parallel is still open for discussion.
Regarding expression of other nuclear-encoded chloroplast proteins, co-regulation with the redox state of the PQ
pool has been demonstrated for cab genes in unicellular
green algae (Escoubas et al., 1995; Maxwell et al., 1995).
A more detailed recent study (Chen et al., 2004) demonstrates that, in the case of Dunaliella tertiolecta, PQdependent modulation of lhcb1 expression starts only 8 h
after modifying the PQ redox state. Immediately after
inducing the redox shift in the PQ pool the trans-thylakoid
membrane potential is the predominant regulator of gene
expression. The long lag phase suggests that expression of
signal transduction elements and proteins involved in the
co-ordination of a regulatory network is necessary for
establishing the correlation between gene activity and the
redox state of the PQ pool.
In higher plants, only weak indication for PQ-dependent
regulation of genes for light-harvesting complex proteins
(LHCP) is available. For cab genes, encoding LHCP of
photosystem II, PQ-dependent regulation has been experimentally excluded for winter rye by Pursiheimo et al.
(2001), who describe a correlation of gene expression with
the acceptor availability of photosystem I. In addition, PQdependent redox regulation was not observed for nuclear
encoded psaF and psaD expression in mustard seedlings
(Pfannschmidt et al., 2001b). Interestingly, even in the case
of petE2, which to date is the model gene for the regulation
of nuclear gene expression by the PQ redox state, other
Chloroplast redox regulation
signals such as the sugar status (Oswald et al., 2001),
phytochrome-A (Dijkwel et al., 1997) and abscisic acid
(Huijser et al., 2000) are dominant regulators in Arabidopsis
thaliana. In pea and tobacco, PQ-dependent regulation is
overwritten and antagonized post-translationally by a PETdependent signal (Sullivan and Gray, 2002). It is tempting to
assume that the PQ signal, which is central in regulating state
transition (Allen, 1992) and chloroplast transcription of
photoreaction centre proteins (Pfannschmidt et al., 1999), is
of minor importance for chloroplast-to-nucleus signalling in
mature leaves and under most environmental circumstances.
According to the gradual model of redox signalling proposed
by Pfannschmidt et al. (2001a) PQ triggers the signalling
pathway with the highest sensitivity and lowest threshold
to redox imbalances. Based on the data available, PQdependent signalling appears to have an ancillary or
insignificant role in controlling the genetic responses to
metabolically relevant redox imbalances in green tissues
under ambient growth conditions and moderate stress. This
conclusion is supported by a recent study in which regulation
of gene expression in response to PQ redox state has been
studied on a transcriptome level (Fey et al., 2005). Although
small sets of genes have been identified as being responsive
to the PQ redox state, the experiments were performed at
photon flux densities of less than 40 lmol mÿ2 sÿ1, i.e.
conditions that barely have major relevance for regulatory
adjustment of photosynthesis under natural conditions.
At higher light intensities (a cloudy day corresponds to
100–300 lmol mÿ2 sÿ1and a sunny day to 1500–2000 lmol
mÿ2 sÿ1) the PQ pool is intermediately reduced under most
conditions. However, in the vascular tissues and their bundle
sheaths, where the redox state of the PQ pool may be
controlled more strongly by NADPH-dependent, presumably NDH-mediated reduction (Peltier and Cournac, 2002),
a signalling function is more likely. Therefore, expression of
cytosolic apx2, which is preferentially expressed along the
main veins (Ball et al., 2004), may correlate with the PQ
redox state (Yabuta et al., 2004) as well as with the cellular
redox status (Chang et al., 2004) and the availability of low
molecular weight antioxidants (Ball et al., 2004).
Thioredoxin-mediated signals: At the acceptor site of photosystem I, ferredoxin-thioredoxin reductase reduces thioredoxins (Trx) depending on the electron pressure and the
reduction state of ferredoxin (Fridlyand and Scheibe, 1999).
A genome-wide survey showed various chloroplast thioredoxins, namely four Trx-m, two Trx-f, two Trx-y, and one
Trx-x (Collin et al., 2004). Together with other small redox
proteins like glutaredoxins (Rouhier et al., 2004) and
cyclophilins (Romano et al., 2004) they mediate thioldisulphide redox interchange of various chloroplast proteins like fructose-1,6-bisphosphase, malate dehydrogenase,
peroxiredoxins, and the RB60-protein with partly overlapping specificity. The redox states of the target proteins
modulate the chloroplast metabolite fluxes, ATP synthesis,
1455
the release of reduction energy into the cytosol, the
chloroplast peroxidase activity and chloroplast translation
(Schürmann, 2003; König et al., 2002; Barnes and Mayfield, 2003). As indicated by the spectrum of target proteins
(Motohashi et al., 2001), redox regulation depending on the
redox state of thioredoxins is manifold and far from being
understood comprehensively. In this context, the classification of Trx function as signal, sensor or transmitter of
redox information depends on definition. The reduction
state of thioredoxin is an indicator of redox state and thus
a transmitter for subsequent signal generation by downstream events rather than the signal or sensor itself. The
sink capacity for consumption of reduction energy of the
thiol system is determined by the auto-oxidation rate of
target proteins (Schürmann, 2003) and, in case of peroxiredoxins, by the rates of peroxide reduction (König et al.,
2002). Electron drainage into the thioredoxin pathways
withdraws electron from ferredoxin:NADP+-reductase and
the Mehler reaction (Fridlyand and Scheibe, 1999) and thus
competes with the generation of ROS and possible (reductive) signals in metabolic pathways. The allocation of
electrons between the different metabolic sinks has to be
adjusted for optimal assimilation rate versus dissipation of
excess energy. For example, peroxides produced in the
Mehler reaction are detoxified by ascorbate peroxidase or
peroxiredoxin yielding dehydroascorbic acid and oxidized
peroxiredoxin, respectively. Through the regeneration of
reduced ascorbate and peroxiredoxin, both reaction sequences consume further reductive power and relieve
electron pressure in the PET chain (Fortis and Elli, 1996;
Dietz et al., 2002). Redox information must be central in
the regulation of these processes.
Photosynthates and the plastidic redox state of NADPH/
NADP+: The photosynthetic electron transport drives reductive metabolism. Therefore, basically any metabolite
synthesized, depending on the availability of reducing
energy, could be a redox signal. Examples for putative
signalling metabolites are carbohydrates (‘sugar sensing’),
which are synthesized in photosynthesis and consumed in
mitochondria by respiration depending on the cellular
energy status (‘energy sensing’). Channelling reduction
energy between chloroplasts and mitochondria can protect
photosynthesis against photoinhibition (Saradadevi and
Raghavendra, 1992). In light-enhanced dark respiration,
malate is the preferred redox transmitter (Padmasree et al.,
2002). NADH generated by dehydrogenase activity is
fed into the respiratory electron transport chain and the
alternative oxidase branch (Gardeström et al., 2002). It is
open for debate if and how sensing of the cytosolic
carbohydrate concentration interferes with redox signalling.
Sugar signalling involves, for example, hexokinase (Jang
et al., 1997), which drives the expression of various
nuclear-encoded chloroplast proteins, including suppression of Rubisco, light-harvesting complex proteins, and
1456 Baier and Dietz
seduheptulose bisphosphatase (Moore et al., 2003), and
SNF1-like kinases (Halford et al., 2003). Some of the target
genes, for example, lhcb1 (cab3) and petE2, are also model
genes in the analysis of redox signalling (see above). In
addition to stimulating respiration, carbohydrate fluxes
between chloroplast and cytosol mediate the exchange of
information on the chloroplast redox state. Two wellstudied examples for redox valves controlled by carbohydrate metabolism are the malate-oxaloacetate shuttle and
the triose phosphate/3-phosphoglycerate shuttle (Heineke
et al., 1991) (Fig. 2). Both transporters exchange redox
energy between the chloroplastic NADPH and the cytosolic
NADH-system. Since the chloroplastic NADPH/NADP+
ratio is about 0.5 in the light and the cytosolic NADH/
NAD+ ratio about 10ÿ3 (Heineke et al., 1991), the transport
is essentially unidirectional due to photosynthetic activity
and depends on the photosynthetic electron pressure
(triose-phosphate/3-phosphoglycerate shuttle) and Trxdependent enzyme activation (malate valve).
Other putative signalling molecules are amino acids,
whose biosynthesis provides a strong electron sink by the
high consumption of reduction energy in carbohydrate
biosynthesis and nitrate reduction. That the signalling pathways, which are presently under investigation (Palenchar
et al., 2004), could have an impact on chloroplast redox
signature is, for example, indicated by co-regulation of the
ferredoxin gene At2g27510 and the two ferredoxin-NADP+reductases At1g30510 and At4g05390. Expression of the
proteins, which are involved in distributing electrons from
the photosynthetic light chain to NADP+, is controlled by
a carbon/nitrogen signalling pathway with dominance of the
carbon component (Palenchar et al., 2004).
Analyses of lhcb1 transcription in winter rye and of
2-Cys Prx (2CPA) in Arabidopsis thaliana indicate
Fig. 2. The malate-oxaloacetate and the triose-phosphate-shuttle link
the chloroplast NADPH pool with the cytosolic NADH-pool. 3-PGA,
3-phosphoglycerate; 1,3-bPGA, glycerate-1,3-bisphosphate; DHAP, dihydroxyacetonephosphate; GAP, glyceraldehyde-3-phosphate (figure
adapted from Heineke et al., 1991. ªThe American Society of Plant
Biologists, with permission).
regulation by the redox state of chloroplast NADPH/
NADP+ (Pursiheimo et al., 2001; Baier et al., 2004).
However, transcriptional activity of cab genes and 2CPA
is distinctly regulated in response to photosynthates. While
transcription of lhcb1 is suppressed by sugars via the
hexokinase-dependent pathway (Moore et al., 2003),
regulation of 2CPA is independent of sugar signalling
(Baier et al., 2004). Low concentrations of externally
applied sugars even increases 2CPA promoter activity by
10–20%. The dominance of redox-regulation of 2CPA was
demonstrated by low 2CPA-promoter driven reporter gene
activity in the presence of strong electron sinks such as
CO2 and NOÿ
3 (Baier et al., 2004). Since the inhibition of
PET also decreased the promoter activity, regulation
depends on photosynthetic activity. Apparently, the acceptor availability of photosystem I, possibly mediated by
the redox state of the NADPH/NADP+-system, controls
the promoter activity (Baier et al., 2004).
External application of millimolar amounts of peroxides
only slightly increased 2CPA transcript amount (Baier and
Dietz, 1997; Horling et al., 2003; Baier et al., 2004),
while a strong up-regulation was seen upon wounding
which rapidly and efficiently suppresses photosynthetic
activity (Chang et al., 2004). These data support the view
that the regulatory redox signal is of chloroplast origin.
Pharmacological studies suggest that signal transduction
takes place via protein kinases. In the expressional
inhibition under reducing conditions a staurosporinesensitive serine/threonine kinase is involved, while under
oxidizing conditions a PD98059-sensitive MAPKK transmits the signal (Horling et al., 2001; Baier et al., 2004).
The analysis of Arabidopsis mutants with lower induction
of 2CPA, the rimb-mutants, suggests that chloroplast
monodehydroascorbate reductase, stromal ascorbate peroxidase, chloroplast CuZn superoxide dismutase csd2,
and plastidic malate dehydrogenase are modulated by
components of the signalling pathway triggering 2CPA
expression (I Heiber and M Baier, unpublished results).
Abscisic acid and violaxanthin-cycle activity: In case of
2CPA gene expression, redox regulation of transcription
depends on the plant hormone abscisic acid (ABA) (Baier
et al., 2004). In addition, ABA-responsive cis-elements are
found in promoters of many nuclear-encoded chloroplast
proteins (Weatherwax et al., 1996; Milla et al., 2003). The
close interrelation between ABA signalling and photosynthesis is indicated by the isolation of alleles for ABAbiosynthetic enzymes and for ABA signal transduction
elements in screens for mutants impaired in the expression
of the plastocyanin gene petE2 (Huijser et al., 2000) and
the gene for a regulatory subunit of ADP-glucose pyrophosphorylase (apL3; Rook et al., 2001). PetE2 (Huijser
et al., 2000) is like 2CPA (Baier et al., 2004) suppressed by
ABA, while apL3 (Rook et al., 2001) is like apx2 (Chang
et al., 2004) ABA-induced (Fig. 3).
Chloroplast redox regulation
thylakoid lumen
H+
Asc
AscH
thylakoid
neoxanthin
chloroplast stroma
NCED
violaxanthin
VDE
DHA
antheraxanthin
ZE
xanthoxin
NADP+
1457
cytosol
xanthoxin
ABA aldehyde
NADPH
zeaxanthin
H+
H+ + O2
PS-I
ABA
NADPH
+
NADP
PS-II
ROS
Asc
H2O
DHA
DHA
GSH
Asc
Asc
GSSG
DHA
NADP+
ROS
Transcription
apx2, apL3
2CPA, petE2
NADPH
Fig. 3. Regulation of ABA biosynthesis by photosynthesis. Violaxanthin de-epoxidase (VDE) acitivity is stimulated by thylakoid acidification and
driven by the availability of protonated, reduced ascorbate (AscH), while zeaxanthin epoxidase (ZE) depends on NADPH. Under photo-oxidizing
conditions, detoxification of ROS can limit VDE due to increased oxidation of ascorbate (Asc) to dehydroascorbate (DHA). 9-cis-epoxycarotenoid
dioxygenase (NCED) catalyses xanthoxin synthesis from neoxanthin and violaxanthin. In the cytosol ABA is synthesized in two steps from xanthoxin
and regulates nuclear gene expression by triggering a specific signalling cascade.
ABA biosynthesis starts inside the chloroplast and
depends on xanthoxin synthesized from violaxanthin
and the violaxanthin-derivative neoxanthin (Finkelstein
and Rock, 2002) (Fig. 3). Most of the violaxanthin within
the thylakoid membrane takes part in the xanthophyll cycle,
which is a redox reaction system of reversible xanthophyll
epoxidation and de-epoxidation (Eskling et al., 1997). In
excess light, the xanthophyll cycle is activated for the
dissipation of excess energy. De-epoxidation of violaxanthin to zeaxanthin via antheraxanthin requires reduced and
protonated ascorbic acid in the thylakoid lumen (Bratt
et al., 1995), which makes it not only dependent on the
ascorbate content, but also on the redox state of the
ascorbate pool. Regeneration of ascorbate is covered by
the NADPH-dependent Halliwell–Foyer cycle (Foyer and
Halliwell, 1977). However, if dehydroascorbate reduction
cannot keep pace with ascorbate oxidation, the xanthophyll
cycle gets uncoupled. If violaxanthin accumulates, it may
promote ABA synthesis. The hypothesis on the regulation
of ABA-biosynthesis by ascorbate availability is supported
by the characterization of the ascorbate biosynthetic mutant
vtc1 (Pastori et al., 2003). In leaves, which accumulate only
30% of wild-type ascorbate (Conklin et al., 1997), the ABA
content was increased by 60% (Pastori et al., 2003). In
parallel, the expression of 9-cis-epoxycarotenoid dioxygenase (NCED) increased (Pastori et al., 2003), which catalyses the irreversible oxidative cleavage of neoxanthin and/
or violaxanthin to xanthoxin (Finkelstein and Rock, 2002),
indicating that ABA biosynthesis in a low ascorbate
background is also promoted by the adaptation of gene
expression.
The thylakoid lumen is especially sensitive to limitations in ascorbate availability since it depends on noncatalysed diffusion of ascorbate through the thylakoid
membrane (Foyer and Lelandais, 1996). The supply with
reduced ascorbate to the lumen is affected by the local
redox poise on the stromal site, where, for example, the
Mehler reaction and ascorbate peroxidase activity strain
the ascorbate pool. The redox regulation of ABA
biosynthesis dependent on PET is further enhanced by
redox-regulation of ABA signal transduction, as oxidative
inhibition of the ABA antagonistic phosphatases ABI1
and ABA2 (Meinhard and Grill, 2001; Meinhard et al.,
2002) increases ABA sensitivity.
The oxidative stimulation of ABA biosynthesis and
ABA signal transduction has a different impact on the
expression of various antioxidant enzymes. For example,
transcript levels of cytosolic ascorbate peroxidase apx2 are
up-regulated by ABA (Cheong et al., 2004). As a consequence of ABA-induced H2O2 generation, apx2 is induced
under photoinhibitory conditions (Chang et al., 2004).
High activity of the antioxidant enzyme helps to balance the
cytosolic redox poise, as long as the cytosolic ascorbate
availability is sufficient to support H2O2 reduction. Thus, it
is assumed that the chloroplast ABA signal synergistically increases the cytosolic antioxidant capacity before
the extraplastidic compartments are flooded with photooxidatively produced ROS. In addition to cytosolic apx2
(Chang et al., 2004), chloroplastic gpx1 is induced by ABA
(Milla et al., 2003). GPx1 acts independently of ascorbate by using reduced glutathione as a co-factor, which
can more efficiently be regenerated inside the chloroplast
by glutathione reductase at the expense of NADPH (Baier
et al., 2000; Noctor et al., 2000). Under photoinhibitory
conditions, increased amounts of Gpx1 may substitute
for chloroplast ascorbate peroxidase, which is susceptible
to shifts in the redox poise of ascorbate (Miyake and
Asada, 1996).
1458 Baier and Dietz
Expression of 2CPA, which is a peroxidase reducing
a broad range of peroxides independent of low-molecularweight antioxidants as co-factors (Baier and Dietz, 1999a,
b; König et al., 2003) is suppressed by ABA (Baier et al.,
2004). The antagonism of oxidative induction and ABA
suppression may keep the transcript and protein on fairly
constant, but high, levels under most growth conditions
including stress situations (Baier and Dietz, 1996, 1997;
Horling et al., 2003; Baier et al., 2004). Exceptions are
observed under severe stresses like wounding (Baier et al.,
2004) and limitations in thioredoxin regeneration (Keryer
et al., 2004), which is needed for driving peroxiredoxin
activity (König et al., 2002). Biochemical analysis of 2-Cys
Prx in barley (König et al., 2003) demonstrated that under
stress conditions increasing portions of the active site of the
enzyme get over-oxidized. The oxidation causes conformational changes leading to decamerization and attachment
of the inactive enzyme to the thylakoid membranes (König
et al., 2003). Ongoing work with transgenic Arabidopsis
thaliana lines and in vitro studies with isolated thylakoids
and heterologously expressed PRX suggest that the binding
of 2-Cys Prx to the thylakoid membrane modulates PET
(P Lamkemeyer, WX Li, M Laxa, K-J Dietz, unpublished
results). As outlined above, 2CPA expression is antagonistically regulated by negative inputs through ABA and
reductive stimuli, and positive input by oxidative stimuli.
This mechanism reduces the rates for re-synthesis of active
enzyme under stress conditions (Fig. 4). Another explanation for ABA-dependent suppression of 2CPA may be
linked to its substrate spectrum. Prx reduces a wide range of
alkyl hydroperoxides (König et al., 2002) some of which
are precursors for oxolipid biosynthesis (Blée and Joyard,
1996). Consistent with the finding by Andersson and coworkers (2004) that disruption of AtMYC2, which encodes
a transcription factor positively regulating ABA-responses,
resulted in elevated expression of jasmonate responsive
genes, ABA-suppression of 2CPA may lead to stimulated
rates of jasmonate synthesis.
Perspectives
In the context of photosynthesis and in the regulation of
antioxidant enzymes, chloroplasts act both as source and
target of redox regulation. They are tightly integrated in
cellular metabolism, a fact that often complicates the
experimental dissecting of signal transduction pathways
and pinpointing the causes and consequences of regulatory
reactions. During evolution, the endosymbiont maintained
its photosynthetic capacity with all the associated potential
oxidative hazards. However, most structural and functional
genes were transferred from the plastome to the nucleus,
including all antioxidant and most regulatory genes. A
sophisticated network of regulation evolved composed of
anthero- and retrograde signalling pathways with significant crosstalk and efficient feedback.
gene expression
NADPH
chloroplast
2-Cys Prx
ABA
nucleus
ROS
ROS
ROOH
ROH
Oxolipins
cytosol
cytosolic
antioxidant
defence
Fig. 4. 2-Cys peroxiredoxins as source and target for redox regulation.
2-Cys Prx are nuclear encoded chloroplast peroxidases, which reduce
alkylhydroperoxide (ROOH). Under photo-oxidative stress conditions,
the active site of the enzyme gets inactivated by over-oxidation. Conformational changes lead to decamerization of 2-Cys peroxiredoxin and
thylakoid attachment. Gene expression is regulated by the redox poise of
NADPH/NADP+, ROS, and abscisic acid (ABA), with increasing amounts
of NADPH and ABA repressing the promoter activity and higher oxidation
of the NADPH/NADP+-system and ROS inducing it. The oxolipin
jasmonic acid and salicylic acid, whose biosynthesis can possibly be
regulated by 2-Cys Prx-dependent reduction of alkyl hydroperoxides, do
not directly influence promoter activity. However, they could, like ABA,
increase the oxidative strain on the cytosolic redox environment.
In chloroplasts, antioxidant enzymes came together
from different evolutionary origins (Asada, 2000). They
have been adapted for their function in protecting against
the risks of oxygenic photosynthesis, while the oxygen
concentration and light intensities increased. Together
with the chloroplast targeting signals, the promoters have
evolved. From double targeting of the antioxidant enzymes glutathione reductase, ascorbate peroxidase, and
monodehydroascorbate reductase into chloroplasts and
mitochondria (Chew et al., 2003) it has to be assumed
that this process is still ongoing. 2-Cys peroxiredoxins
and glutathione peroxidase already show compartmentspecific targeting and regulation (Baier and Dietz, 1997;
Mullineaux et al., 1998). For 2-Cys peroxiredoxin-A,
which is very likely of endosymbiotic origin (Baier and
Dietz, 1997), by taking over an ancient function in the
protection of the photosynthetic membrane, promoter
adaptation closed a regulatory circuitry of multi-level
redox regulation, in which the chloroplast enzyme is the
source and the target of redox regulation (Fig. 4).
Analysis of the gpx gene structures (Milla et al., 2003)
points to the multiplication of a single ancestor gene.
Only gpx1 transcripts, which encode the chloroplast
isoforms, are induced by ABA and gpx1 is, besides
gpx6, the only gpx gene not responding to the oxolipin
derivates jasmonic acid and salicylic acid (Milla et al.,
2003). The regulation pattern indicates specific responses
to second messengers generated by chloroplast metabolism by moderate (ABA) and strong (oxolipins) redox
imbalances.
Chloroplast redox regulation
Acknowledgement
Parts of our own work presented here were supported by the DFG
(FOR 387 TP3 and Ba2011/2).
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