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
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 retro-
grade signals has emerged to co-ordinate the activities
of the different genetic and metabolic compartments. A
major focus of recent research in chloroplast regula-
tion addressed the mechanisms of redox sensing and
signal transmission, the identification of regulatory
targets, and the understanding of adaptation mech-
anisms. 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 avail-
ability at photosystem I, in addition to control by
oxolipins, tetrapyrroles, carbohydrates, and abscisic
acid. The signalling function is discussed in the con-
text of regulatory circuitries that control the expression
of antioxidant enzymes and redox modulators, demon-
strating 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.
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< ?900 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 O2in the so-called Mehler reaction (Mehler,
1951). The superoxide radicals formed can be quickly
converted into H2O2and highly reactive hydroxyl radicals
(HOc) (Elstner, 1990). Together with reactive oxygen
species (ROS) generated by other sources, they are a con-
tinuous threat to cellular constituents for uncontrolled
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, chloro-
plasts are prone to oxidative damage like no other organelle
(Foyer et al., 1997). Consequently, photosynthetic organ-
isms have evolveddefence mechanismsto control the redox
poise of the electron transport chain and the redox envir-
onment of the stroma. They range from the suppression of
* To whom correspondence should be addressed. Fax: +49 (0)521 106 6039. E-mail: Margarete.Baier@uni-bielefeld.de
Abbreviations: 2CPA, 2-Cys peroxiredoxin A; ABA, abscisic acid; DBMIB, 3-methyl-6-isopropyl-p-benzoquinone; DCMU, 3-(39,49-dichlorophenyl-)1,1-
dimethyl 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.
Journal of Experimental Botany, Vol. 56, No. 416, pp. 1449–1462, June 2005
doi:10.1093/jxb/eri161Advance Access publication 29 April, 2005
ª The Author . Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For Permissions, please e-mail: firstname.lastname@example.org
ROS generation and avoidance of uncontrolled oxidation of
essential biomolecules by accumulating high concentra-
tions of low-molecular weight antioxidants to repair mech-
anisms 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 elec-
trons 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 ?300 mV to approximately ?240 mV; Dietz,
2003). Under these conditions, chloroplasts stabilize their
redox poise by metabolization of starch and import of
Studies with various transgenic plant lines and mutants
demonstrated the importance of a high antioxidant cap-
acity 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 re-
sponds to redox imbalances. The pool size of low molecu-
lar 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 O2that, 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 low-
molecular-weight antioxidants are nuclear encoded. The
spatial separation of expression and function demands for
signal transduction over the chloroplast envelope. Devia-
tions 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
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,
may have additional functions, for example, as a metabolic
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 antioxi-
dants, the redox state of a particular compound is under the
Enzymes lower the kinetic barriers and couple redox pairs.
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 un-
couple the redox states of individual components of the
took place in catalase-deficient barley (Willekens et al.,
1997), reduced 2-Cys peroxiredoxin levels led preferen-
tially 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
redox homeostasis and redox metabolism, the nature of
a particular antioxidant employed in a specific detoxifica-
tion reaction and, within limits, the relative redox state of an
Fig. 1. The cytosolic antioxidant system shields the nucleus from chloro-
plast 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.
1450 Baier and Dietz
individual antioxidant may be of minor importance. How-
ever, deviations from redox normality can serve in signal
generation and signal transmission.
Defining redox signals in the context of
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 chloro-
plasts and the nucleus for experimental and thematic
reasons. (i) The metabolic state of chloroplast metabolism
can easily be manipulated by altering exogenous param-
eters 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 expres-
sion and regulates the photosynthetic capacity during long-
term adaptation (Dietz, 2003). However, the hypothesis,
on retrograde redox signalling originating inside chloro-
plasts, is generally accepted and despite these systematic
advantages, the precise nature of the signals, their speci-
ficity and interaction are only recently becoming tangible.
Theoretical considerations and experimental data have
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
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 cross-
talk with other signalling cascades. Other definitions for
to photosynthetic electron pressure (Pfannschmidt et al.,
2001a) or on their putative initiation sites (Pfannschmidt
et al., 2003). For chloroplast-to-nucleus signalling, which
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
cellular redox components or by ROS are distinguished
from signals transmitted by second messengers synthesized
inside chloroplasts (Fig. 1).
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 stress-
ors, low availability of antioxidants, and by antioxidant
feeding, respectively. The common feature of all these
treatments is that the cytosolic redox environment speci-
fically 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, monitor-
ing 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 H2O2and that from shifts in the
redox poise of low-molecular-weight antioxidants. There-
fore, 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 regu-
lation of transcript amounts in the low-ascorbate mutant
vtc1 and Vandenabeele et al. (2004) that in a catalase-
deficient tobacco line, as well as Davletova et al. (2005)
that of a knock-out mutant of cytosolic ascorbate peroxi-
dase APx1, and Ball et al. (2004) determined the transcrip-
tional 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 antioxi-
dant 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).
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
Chloroplast redox regulation1451
(CACGTG; Schindler et al., 1992) and ABRE-type
(BACGTGKM; Shinozaki and Yamaguchi-Shinozaki,
2000), Myb (AtMyb1: MTCCWACC; AtMyb2: TAACS-
GTT; 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 diphos-
phate kinase AtNDPK2 in Arabidopsis thaliana. By stimu-
lation 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 antag-
onistic phosphatase activities (Mittler et al., 2004).
In addition to MAPK signalling, thiol-disulphide tran-
sitions can control gene expression in response to ROS
accumulation and changes in the cellular thiol homeo-
stasis. 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) (Despre ´s
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 reduc-
tion 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 antioxidant-
dependent 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 c-
glutamyl 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 differ-
entially 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 ac-
tivity 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 trans-
mission by micro-bursts.
For the regulation of nuclear-encoded chloroplast anti-
oxidant enzymes, transcriptome analysis (Kimura et al.,
2003; Davletova et al., 2005), the analysis of transcript
amount for the regulation of chloroplast ascorbate perox-
idase (Yoshimura et al., 2000), the chloroplast peroxire-
doxins (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 non-
plastidic antioxidant enzymes. However, in 2-Cys peroxi-
redoxin 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 thyla-
koid ascorbate peroxidase were selectively induced (Baier
et al., 2000). Loss of 2-Cys peroxiredoxin function led to
slight photoinhibition, damage of the photosynthetic mem-
brane, and oxidation of the ascorbate pool, suggesting
photo-oxidative stress (Baier and Dietz, 1999b). The fact
that three transcripts for chloroplast antioxidants accumu-
1452 Baier and Dietz
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 thresh-
old 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 antioxi-
dants that are decomposed or reduced, respectively, during
diffusion through the cell. In respect of chloroplast-to-
nucleus signalling, several putative signals have been
suggested, of which some will be discussed here.
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 caroten-
oid biosynthesis suppressed the expression of various
nuclear-encoded chloroplast proteins, for example, Lhcb1,
PsbR, RbcS, PetH, and PetE, during early seedling de-
velopment (Harpster et al., 1984; Mayfield and Taylor,
1984; Bolle et al., 1994; Gray et al., 1995). Based on these
observations, retrograde chloroplast signals were hypothe-
sized 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 Mg-
chelatase (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 d-
aminolevulinic 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 Glu-
tRNA reductase at the C-terminus (Goslings et al., 2004).
Characterization of the mutant ulf3, which is allelic to gun2
(Susek et al., 1993), demonstrated that tetrapyrrole bio-
synthesis 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 accu-
mulate protoporphyrin-IX, that imbalances in tetrapyrrole
biosynthesis primarily lead to modulation of gene expres-
sion by photosensitization of the pigments. Redox signals,
for example, H2O2accumulation or shifts in the redox state
of low-molecular-weight antioxidants, may be involved in
the suppression of nuclear gene expression in norflurazone-
treated 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 photosyn-
thetic electron transport (Sullivan and Gray, 2002), pre-
sumably 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).
Besides oxidatively damaged tetrapyrroles, oxolipins are
dependent 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 con-
ditions by oxidation of unsaturated fatty acids either
mediated by ROS (Ble ´e 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 antioxi-
dant defence is close to oxidative collapse. Various plant
signalling molecules are synthesized from alkyl hydroper-
oxides (Ble ´e and Joyard, 1996). Jasmonates, which are
a group of 12-carbon fatty acid cyclopentanones and dinor-
oxo-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.
Chloroplast redox regulation1453
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 glutathi-
one peroxidases (gpx1 and gpx7), of which only gpx1 is
expressed(Milla et al., 2003), and four openreading frames
for chloroplast peroxiredoxins (Horling et al., 2003).
Peroxiredoxins and gpx1 are induced by H2O2and butyl-
hydroperoxide (Horling et al., 2003; Avsian-Kretchmer
et al., 2004) indicating that their expression possibly
antagonizes oxolipin signal formation. However, expres-
sion 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.
Peroxideformation andreductionmaybe furtheruncoupled
due to the sensitivity of the active site cysteine residues to
over-oxidation. 2-Cys Prx have been suggested to func-
tion as flood gates that normally keep peroxides at a low
level (Wood et al., 2003; Ko ¨nig 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 H2O2and 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 (Ko ¨nig et al., 2003). Therefore, with the
accumulation of alkyl hydroperoxides, oxolipin biosyn-
thesis may get increasingly dependent on LOX-, DOX-,
In recent years various mutants with decreased sensitiv-
ity 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 investi-
gated 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
Photosynthetically controlled signals
The redox state of the plastoquinone pool: Efficient regula-
tion 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 photosys-
tem II mediates electron transfer between photosystem II
and the cytochrome b6f-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 presum-
ably by binding of plastoquinol to the cytochrome b6f-
complex (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 chloro-
plast 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) demon-
strates that, in the case of Dunaliella tertiolecta, PQ-
dependent 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 experi-
mentally 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, PQ-
dependent 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
1454 Baier and Dietz
signals such as the sugar status (Oswald et al., 2001),
phytochrome-A (Dijkwel et al., 1997) and abscisic acid
thaliana. In pea and tobacco, PQ-dependent regulation is
overwritten and antagonized post-translationally by a PET-
transition (Allen, 1992) and chloroplast transcription of
photoreactioncentreproteins (Pfannschmidt etal.,1999),is
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, PQ-
dependent 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
of gene expression in response to PQ redox state has been
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 m?2s?1, 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
m?2s?1) the PQ pool is intermediately reduced under most
sheaths, where the redox state of the PQ pool may be
controlled more strongly by NADPH-dependent, presum-
ably NDH-mediated reduction (Peltier and Cournac, 2002),
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 photo-
system I, ferredoxin-thioredoxin reductase reduces thio-
redoxins (Trx) depending on the electron pressure and the
reductionstate of ferredoxin(Fridlyand andScheibe,1999).
A genome-wide survey showed various chloroplast thio-
redoxins, 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 thiol-
disulphide redox interchange of various chloroplast pro-
teins like fructose-1,6-bisphosphase, malate dehydrogenase,
peroxiredoxins, and the RB60-protein with partly over-
lapping specificity. The redox states of the target proteins
modulate the chloroplast metabolite fluxes, ATP synthesis,
the release of reduction energy into the cytosol, the
chloroplast peroxidase activity and chloroplast translation
(Schu ¨rmann, 2003; Ko ¨nig et al., 2002; Barnes and May-
field, 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 classifi-
cation 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 down-
stream 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 (Schu ¨rmann, 2003) and, in case of peroxi-
redoxins, by the rates of peroxide reduction (Ko ¨nig 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 (re-
ductive) 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 se-
quences 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 re-
ductive 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 (Gardestro ¨m 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 suppres-
sion of Rubisco, light-harvesting complex proteins, and
Chloroplast redox regulation 1455
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 well-
studied examples for redox valves controlled by carbohy-
drate 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 10?3(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 Trx-
dependent 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 path-
ways, 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
reductases At1g30510 and At4g05390. Expression of the
proteins, which are involved in distributing electrons from
the photosynthetic light chain to NADP+, is controlled by
carbon component (Palenchar et al., 2004).
Analyses of lhcb1 transcription in winter rye and of
2-Cys Prx (2CPA) in Arabidopsis thaliana indicate
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
PET also decreased the promoter activity, regulation
depends on photosynthetic activity. Apparently, the ac-
ceptor 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 staurosporine-
sensitive serine/threonine kinase is involved, while under
oxidizing conditions a PD98059-sensitive MAPKK trans-
mits 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 per-
oxidase, 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).
3(Baier et al., 2004). Since the inhibition of
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 photosyn-
thesis is indicated by the isolation of alleles for ABA-
biosynthetic 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 pyro-
phosphorylase (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).
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, di-
hydroxyacetonephosphate; GAP, glyceraldehyde-3-phosphate (figure
adapted from Heineke et al., 1991.ªThe American Society of Plant
Biologists, with permission).
1456 Baier and Dietz
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 violaxan-
thin 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 dioxygen-
ase (NCED) increased (Pastori et al., 2003), which catal-
yses 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
The thylakoid lumen is especially sensitive to limita-
tions in ascorbate availability since it depends on non-
catalysed 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 conse-
quence of ABA-induced H2O2generation, 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 H2O2reduction. Thus, it
is assumed that the chloroplast ABA signal synergistic-
ally increases the cytosolic antioxidant capacity before
the extraplastidic compartments are flooded with photo-
oxidatively 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 ascor-
bate 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
thylakoid lumen thylakoid
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.
Chloroplast redox regulation1457
Expression of 2CPA, which is a peroxidase reducing
a broad range of peroxides independent of low-molecular-
weight antioxidants as co-factors (Baier and Dietz, 1999a,
b; Ko ¨nig 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 (Ko ¨nig et al., 2002). Biochemical analysis of 2-Cys
Prx in barley (Ko ¨nig et al., 2003) demonstrated that under
stress conditions increasing portions of the active site of the
enzyme get over-oxidized. The oxidation causes conform-
ational changes leading to decamerization and attachment
of the inactive enzyme to the thylakoid membranes (Ko ¨nig
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 antagonis-
tically 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 explan-
ation for ABA-dependent suppression of 2CPA may be
linked to its substrate spectrum. Prx reduces a wide range of
alkyl hydroperoxides (Ko ¨nig et al., 2002) some of which
are precursors for oxolipid biosynthesis (Ble ´e and Joyard,
1996). Consistent with the finding by Andersson and co-
workers (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.
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 signifi-
cant crosstalk and efficient feedback.
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 en-
zymes 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 compartment-
specific 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 metabol-
ism by moderate (ABA) and strong (oxolipins) redox
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. Con-
formational 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
ofNADPH and ABA repressingthe promoteractivity and higheroxidation
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.
1458 Baier and Dietz
Parts of our own work presented here were supported by the DFG
(FOR 387 TP3 and Ba2011/2).
Ahlfors R, Land S, Overmyer K, et al. 2004. Arabidopsis
RADICAL-INDUCED CELL DEATH1 belongs to the WWE
protein–protein interaction domain protein family and modulates
abscisic acid, ethylene, and methyljasmonate responses. The Plant
Cell 16, 1925–1937.
Allen JF. 1992. Protein phosphorylation in regulation of photosyn-
thesis. Biochimica et Biophysica Acta 1098, 275–335.
Asada K. 2000. The water–water cycle as alternative photon and
electron sink. Philosophical Transactions of the Royal Society
London B 355, 1419–1431.
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-
Gomez L, Boller T, Ausubel FM, Sheen J. 2002. MAP kinase
signalling cascade in Arabidopsis innate immunity. Nature 415,
Avsian-Kretchmer O, Gueta-Dahan Y, Lev-Yadun S, Gollop R,
Ben-Hayyim G. 2004. The salt-stress signal transduction pathway
that activates the gpx1 promoter is mediated by intracellular H2O2,
different from pathway induced by extracellular H2O2. Plant
Physiology 135, 1685–1696.
Baier M, Dietz K-J. 1996. Primary structure and expression of plant
homologues of animal and fungal thioredoxin-dependent peroxide
reductases and bacterial alkyl hydroperoxide reductases. Plant
Molecular Biology 31, 553–564.
Baier M, Dietz K-J. 1997. The plant 2-Cys peroxiredoxin BAS1 is
a nuclear-encoded chloroplast protein: its expressional regulation,
phylogenetic origin, and implications for its specific physiological
function in plants. The Plant Journal 60, 282–314.
Baier M, Dietz K-J. 1998. The costs and benefits of oxygen for
photosynthesizing cells. Progress in Botany 60, 282–314.
Baier M, Dietz K-J. 1999a. Alkyl hydroperoxide reductases: the
way out of the oxidative breakdown of lipids in chloroplasts.
Trends in Plant Science 4, 166–168.
Baier M, Dietz K-J. 1999b. Protective function of chloroplast 2-
cysteine peroxiredoxin in photosynthesis. Evidence from trans-
genic Arabidopsis. Plant Physiology 119, 1407–1414.
Baier M, Noctor G, Foyer CH, Dietz KJ. 2000. Antisense
suppression of 2-Cys peroxiredoxin in Arabidopsis specifically
enhanced activities and expression of enzymes associated with
ascorbate metabolism but not glutathione metabolism. Plant
Physiology 124, 823–832.
Baier M, Stro ¨her E, Dietz KJ. 2004. The acceptor availability at
photosystem I and ABA control nuclear expression of 2-Cys
peroxiredoxin-A in Arabidopsis thaliana. Plant and Cell Physi-
ology 45, 997–1006.
Ball L, Accotto G-P, Bechtold U, et al. 2004. Evidence for a direct
link between glutathione biosynthesis and stress defense gene
expression in Arabidopsis. The Plant Cell 16, 2448–2462.
Barnes D, Mayfield SP. 2003. Redox control of post-transcriptional
processes in the chloroplast. Antioxidants and Redox Signaling 5,
Beale SJ. 1999. Enzymes in chlorophyll biosynthesis. Photosyn-
thesis Research 60, 43–73.
BergerS,BellE,MulletJE.1996. Two methyl jasmonate-insensitive
mutants show altered expression of AtVsp in response to methyl
jasmonate and wounding. Plant Physiology 111, 525–531.
Blankenship RE. 2002. Molecular mechanisms of photosynthesis.
Ble ´e E, Joyard J. 1996. Envelope membranes from spinach
chloroplasts are a site of metabolism of PUFA hydroperoxides.
Plant Physiology 110, 445–454.
Bolle C, Sopory SL, Lu ¨bberstedt T, Klo ¨sgen R, Herrmann RG,
Oelmu ¨ller R. 1994. The role of plastids in the expression of
nuclear genes for thylakoid proteins studied with chemirc
b-glucuronidase gene fusions. Plant Physiology 105, 1355–1364.
Bratt CE, Arvidsson P-O, Carlsson M, A˚kerlund H-E. 1995.
Regulation of violaxanthin de-epoxidase activity by pH and
ascorbate concentration. Photosynthesis Research 45, 169–175.
Chang CC-C, Ball L, Fryer MJ, Baker NR, Karpinski S,
Mullineaux PM. 2004. Induction of ASCORBATE PEROXIDASE
2 expression in wounded Arabidopsis leaves does not involve
known wound-signalling pathways but is associated with changes
in photosynthesis. The Plant Journal 38, 499–511.
Chen YB, Durnford DG, Koblizek M, Falkowski PG. 2004.
Plastid regulation of Lhcb1 transcription in the chlorophyte alga
Dunaliella tertiolecta. Plant Physiology 136, 3737–3750.
Chen W, Provart NJ, Glazebrook J, et al. 2002. Expression profile
matrix of Arabidopsis transcription factor genes suggests their
putative functions in response to environmental stresses. The Plant
Cell 14, 559–574.
Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S. 2002.
Transcriptional profiling reveals novel interactions between
wounding, pathogen, abiotic stress, and hormonal responses in
Arabidopsis. Plant Physiology 129, 661–677.
Chew O, Whelan J, Millar AH. 2003. Molecular definition of the
ascorbate-glutathione cycle in Arabidopsis mitochondria reveals
dual targeting of antioxidant defenses in plants. Journal of
Biological Chemistry 278, 46869–46877.
Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M,
Knaff DB, Dietz K-J, Issakidis-Bourguet E. 2004. Character-
ization of plastidial thioredoxins from Arabidopsis belonging to
the new y-type. Plant Physiology 136, 4088–4095.
Conklin PL, Pallanca JE, Last RL, Smirnoff N. 1997. L-Ascorbic
acid metabolism in the ascorbate-deficient Arabidopsis mutant
vtc1. Plant Physiology 115, 1227–1285.
Davletova S, Rizhsky L, Liang H, Shengquiang Z, Oliver DJ,
Coutu J, Shulaev V, Schlauch K, Mittler R. 2005. Cytosolic
ascorbate peroxidase 1 is a central component of the reactive
oxygen gene network of Arabidopsis. The Plant Cell 17, 268–281.
deLeon IP, Sanz A, Hamberg M, Castresana C. 2002. Involve-
ment of the Arabidopsis alpha-DOX1 fatty acid dioxygenase
against oxidative stress and cell death. The Plant Journal 29,
Desikan R, AH-Mackerness S, Hancock JT, Neill SJ. 2001.
Regulation of the Arabidopsis transcriptome by oxidative stress.
Plant Physiology 127, 159–172.
Fobert PR. 2003. The Arabidopsis NPR1 disease resistance
protein is a novel cofactor that confers redox regulation of DNA
binding activity to the basic domain/leucine zipper transcription
factor TGA1. The Plant Cell 15, 2181–2191.
Dietz KJ. 2003. Redox control, redox signaling, and redox homeo-
stasis in plant cells. International Reviews in Cytology 228,
Dietz KJ, Horling F, Ko ¨nig J, Baier M. 2002. The function of the
chloroplast 2-cysteine peroxiredoxin in peroxide detoxification
Dijkwel PP, Huijser C, Weisbeek PJ, Smeekens SCM. 1997.
Sucrose control of phytochrome A signaling in Arabidopsis. The
Plant Cell 9, 583–595.
Elstner EF. 1990. Der Sauerstoff: Biochemie, Biologie, Medizin.
Mannheim: BI Wissenschaftsverlag.
Chloroplast redox regulation1459
Escoubas J-M, Lomas M, LaRoche S, Stutios LM, Angell NA,
Mindrinos M, Cho RJ, Oefner PJ, Davis RW, Ausubel FM.
1995. Light intensity regulation of cab gene transcription is
signalled by the redox state of the plastoquinone pool. Proceedings
of the National Academy of Sciences, USA 92, 10237–10241.
Eskling M, Arvidsson P-O, A˚kerlund H-E. 1997. The xantho-
phylls cycle, its regulation and components. Physiologia Planta-
rum 100, 806–816.
Euglem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The
WRKY superfamily of plant transcription factors. Trends in Plant
Science 5, 199–206.
Farmer EE, Weber H, Vollweider S. 1998. Fatty acid signalling in
Arabidopsis. Planta 206, 167–174.
Feussner I, Wasternack C. 2002. The lipoxygenase pathway.
Annual Reviews in Plant Biology 53, 275–297.
Fey V, Wagner R, Bra ¨utigam K, Wirtz M, Hell R, Dietzmann A,
Leister D, Oelmu ¨ller R, Pfannschmidt T. 2005. Retrograde
plastid redox signals in the expression of nuclear genes for
chloroplast proteins of Arabidopsis thaliana. Journal of Biological
Chemistry (online Manuscript M406358200).
Finkelstein RR, Rock CD. 2002. Ascorbic acid biosynthesis and
response. In: The Arabidopsis book. American Society of Plant
Fortis G, Elli G. 1996. Stimulation of photophosphorylation by
ascorbate as a function of light intensity. Plant Physiology 112,
Foyer CH, Halliwell B. 1977. Presence of glutathione and glutathi-
one reductase in chloroplasts—proposed role in ascorbic acid
metabolism. Planta 133, 21–25.
Foyer CH, Lelandais M. 1996. A comparison of the relative rates of
transport of ascorbate and glucose across the thylakoid, chloroplast
and plasmalemma membranes of pea mesophyll cells. Journal of
Plant Physiology 148, 391–398.
Foyer CH, Lelandais M, Kunert K-J. 1997. Photo-oxidative stress
in plants. Physiologia Plantarum 92, 696–717.
Fridlyand LE, Scheibe R. 1999. Controlled distribution of electrons
between acceptors in chloroplasts: a theoretical consideration.
Biochimica et Biophysica Acta 1413, 31–42.
Gardestro ¨m P, Igamberdiev AU, Raghavendra AS. 2002. Mito-
chondrial functions in light and significance to carbon–nitrogen
interactions. In: Foyer CH, Noctor G, eds. Advances in photosyn-
thesis and respiration: photosynthetic nitrogen assimilation and
associated carbon metabolism, Vol. 12. Dortrecht: Kluwer
Academic Press, 151–172.
Goslings D, Meskauskien R, Kim C, Lee KP, Nater M, Apel K.
2004. Concurrent interactions of haem and FLU with Glut RNA
reductase (HEMA1), the target of metabolic feedback inhibition of
tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis
plants. The Plant Journal 40, 957–967.
Gray JC, Sornarajah R, Zabron AA, Duckett CM, Khan MS.
1995. Chloroplast control of nuclear gene expression. In: Mathis P,
ed. Photosynthesis: from light to biosphere, Vol. 3. Dordrecht:
Kluwer Academic Press, 543–550.
Haehnel W. 1984. Photosynthetic electron transport in higher plants.
Annual Review of Plant Physiology 35, 659–693.
Zhang Y. 2003. Metabolic signalling and carbon partitioning: role
of Snf1-related (SnRK1) protein kinase. Journal of Experimental
Botany 54, 467–475.
Halliwell B, Gutteridge JMC. 1999. Free radicals in biology and
medicine. Oxford: Oxford Science Pulications.
Hamberg M, Sanz A, Rodriguez MJ, Calvo AP, Castresana C.
2003. Activation of the PUFA a-dioxygenase pathway during
bacterial infection of tobacco leaves; formation of oxolipins
protecting against cell death. Journal of Biological Chemistry
Harpster MH, Mayfield SP, Taylor WC. 1984. Effects of pigment-
deficient mutants on the accumulation of photosynthetic proteins in
maize. Plant Molecular Biology 3, 59–71.
Heber U. 2002. Irrungen, Wirrungen? The Mehler reaction in the
relation to cyclic electron transport in C3plants. Photosynthesis
Research 73, 223–231.
Heldt HW. 1991. Redox transfer across the inner chloroplast
envelope membrane. Plant Physiology 95, 1131–1137.
2003. Convergence of signalling pathways induced by systemin,
oligosaccharide elicitors, and ultraviolet-B radiation at the level
of mitogen-activated protein kinases in Lycopersicon peru-
Horling F, Baier M, Dietz K-J. 2001. Redox-regulation of the
expression of the peroxide-detoxifying chloroplast 2-Cys peroxi-
redoxin in the liverwort Riccia fluitans. Planta 214, 304–313.
Baier M, Dietz K-J. 2003. Divergent light-, ascorbate-, and
oxidative stress-dependent regulation of expression of the per-
oxiredoxin gene family in Arabidopsis. Plant Physiology 131,
Huijser C, Kortstee A, Pego J, Weisbeek P, Smeekens S. 2000.
The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to
ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in
sugar responses. The Plant Journal 23, 577–585.
Ichimura K, Mizoguchi T, Yoshida R, Shinozaki K. 2000. Various
abiotic stresses rapidly activate Arabidopsis MAP kinases
ATMPK4 and ATMPK6. The Plant Journal 24, 655–665.
Jang J-C, Le ´on P, Zhou L, Sheen J. 1997. Hexokinase as a sugar
sensor in higher plants. The Plant Cell 9, 5–19.
Kanna M, Tamaoki M, Kubo A, et al. 2003. Isolation of an ozone-
insensitive and jasmonate-semi-insensitive Arabidopsis mutant
(oji1). Plant and Cell Physiology 44, 1301–1310.
1997. Photosynthetic electron transport regulates expression of
cytosolic ascorbate peroxidase genes in Arabidopsis during excess
light stress. The Plant Cell 9, 627–640.
Keetman U, Mock HP, Grimm B. 2002. Kinetics of antioxidative
defense responses to photosensitization in porphyrin-accumulating
tobacco plants. Plant Physiology and Biochemistry 40, 697–707.
2004. Characterization of Arabidopsis mutants for the variable
Research 79, 265–274.
Kimura M, Yamamoto YY, Seti M, Sakurai T, Sato M, Abe T,
Yoshida S, Manabe K, Shinozaki K, Matsui M. 2003. Identi-
fication of Arabidopsis genes regulated by high light-stress using
Kliebenstein DJ, Monde R-A, Last RL. 1998. Superoxide dis-
mutase in Arabidopsis: an eclectic enzyme family with disperate
regulation and protein localization. Plant Physiology 118,
Ko ¨nigJ,BaierM,HorlingF,KahmannU,Schu ¨rmannP,DietzK-J.
2002. The plant-specific function of 2-Cys peroxiredoxin-mediated
detoxification of peroxides in the redox-hierarchy of photosyn-
thetic electron flux. Proceedings of the National Academy of
Sciences, USA 99, 5738–5743.
Ko ¨nig J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz K-J.
2003. Reaction mechanism of plant 2-Cys peroxiredoxin: role of
1460 Baier and Dietz
the C-terminus and the quaternary structure. Journal of Biological
Chemistry 278, 24409–24420.
Kovtun Y, Chiu WL, Tena G, Sheen J. 2000. Functional analysis of
oxidative stress-activated mitogen-activated protein kinase cas-
cades in plants. Proceedings of the National Academy of Sciences,
USA 97, 2940–2945.
Larkin RM, Alonso JM, Ecker JR, Chory J. 2003. GUN4,
a regulator of chlorophyll synthesis and intracellular signaling.
Science 299, 902–906.
Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E. 1998.
Functional analysis of regulatory sequences controlling PR-1 gene
expression in Arabidopsis. The Plant Journal 16, 223–233.
Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R. 2004.
Jasmonate-insensitive1 encodes a MYC transcription factor es-
sential to discriminate between different jasmonate-regulated de-
fense responses in Arabidopsis. The Plant Cell 16, 1938–1950.
2001. The role of conserved residues of the WRKY domain in the
DNA-binding of tobacco WRKY family proteins. Bioscience,
Biotechnology and Biochemistry 65, 2428–2436.
Mahalingam R, Gomez-Buitrago AM, Eckardt N, Shah N,
Guevara-Garcia A, Day P, Raina R, Fedoroff NV. 2003.
Characterizing the stress/defense transcriptome of Arabidopsis.
Genome 4, R20.
Martin C, Paz-Ares J. 1997. MYB transcription factors in plants.
Trends in Genetics 13, 67–73.
Mauch F, Mauch-Mani B, Gaille C, Kull B, Haas D, Reimann C.
2001. Manipulation of salicylate content in Arabidopsis thaliana
by the expression of an engineered bacterial salicylate synthase.
The Plant Journal 25, 67–77.
MayfieldSP,TaylorWC.1984. Carotenoid-deficient maize seedlings
fail to accumulate light-harvesting chlorophyll a/b binding protein
(LHCP) mRNA. European Journal of Biochemistry 144, 79–84.
Maxwell DP, Laudenbach DE, Huner NPA. 1995. Redox regula-
tion of light-harvesting complex II and cab mRNA abundance in
Dunaliella salina. Plant Physiology 109, 787–795.
Mehler A. 1951. Studies on the reaction of illuminated chloroplasts.
I. Mechanisms of the reduction of oxygen and other Hill reagents.
Archives in Biochemistry and Biophysics 33, 65–77.
Meinhard M, Grill E. 2001. Hydrogen peroxide is a regulator of
ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Letters
Meinhard M, Rodriguez PL, GrillE. 2002.The sensitivity of ABI2
to hydrogen peroxide links abscisic acid-response regulator to
redox signalling. Planta 214, 775–782.
Meskauskien R, Nater M, Goslings D, Kessler F, op den Camp R,
Apel K. 2001. FLU: a negative regulator of chlorophyll bio-
synthesis in Arabidopsis thaliana. Proceedings of the National
Academy of Sciences, USA 98, 12826–12831.
Milla MAR, Marer A, Huete AR, Gustafson JP. 2003. Glutathione
peroxidase genes in Arabidopsis are ubiquitous and regulated by
abiotic stresses through diverse signalling pathways. The Plant
Journal 36, 602–615.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004.
The reactive oxygen gene network of plants. Trends in Plant
Science 9, 490–498.
Miyake C, Asada K. 1996. Inactivation mechanisms of ascorbate
peroxidase at low concentrations of ascorbate: hydrogen peroxide
decomposes compound I of ascorbate peroxidase. Plant and Cell
Physiology 37, 423–430.
Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. 2001.
Arabidopsis genomes uncoupled 5 (gun5) mutant reveals the
involvement of Mg-chelatase H subunit in plastid-to-nucleus
signal transduction. Proceedings of the National Academy of
Sciences, USA 98, 2053–2058.
Montillet J-L, Cacas J-L, Garnier L, et al. 2004. The upstream
oxylipins profile of Arabidopsis thaliana: a tool to scan for
oxidative stress. The Plant Journal 40, 439–451.
Moon H, Lee B, Choi G, et al. 2003. NDP kinase 2 interacts with
two oxidative stress-activated MAPKs to regulate cellular redox
state and enhances multiple stress tolerance in transgenic plants.
Proceedings of the National Academy of Sciences, USA 100,
Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H, Liu Y-X,
Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis
glucose sensor HXK1 in nutrient, light, and hormonal signalling.
Science 300, 332–336.
Motohashi K, Kondoh A, Stumpp MT, Hisabori T. 2001. A
comprehensive survey of proteins targeted by chloroplast thiore-
doxins. Proceedings of the National Academy of Sciences, USA
Robinson C, Creissen GP. 1998. Identification of cDNAs
encoding plastid-targeted glutathione-peroxidase. The Plant
Journal 13, 375–379.
Noctor G, Veljovic-Jovanovic S, Foyer C. 2000. Peroxide process-
ing in photosynthesis: antioxidant coupling and redox signalling.
Philosophical Transactions of the Royal Society London, Series B
Oswald O, Martin T, Dominy PJ, Graham IA. 2001. Plastid redox
state and sugars: interactive regulators of nuclear-encoded photo-
synthetic gene expression. Proceedings of the National Academy
of Sciences, USA 98, 2047–2052.
Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-
Jovanovic S, Verrier PJ, Noctor G, Foyer CH. 2003. Leaf vita-
min C contents modulate plant defense transcripts and regulate
genes that control development through hormone signaling. The
Plant Cell 15, 939–951.
PadmasreeK, PadmavathiL, Raghavendra AS. 2002.Essentiality
of mitochondrial oxidative metabolism for photosynthesis: opti-
mization of carbon assimilation and protection against photo-
inhibition. Critical Reviews in Biochemistry and Molecular
Biology 37, 71–119.
Palenchar PM, Kouranov A, Lejay LV, Coruzzi GM. 2004.
Genome-wide patterns of carbon and nitrogen regulation of gene
expression validate the combined carbon and nitrogen (CN)-
signalling hypothesis in plants. Genome Biology 5, R91.
Panchuk II, Volkov RA, Scho ¨ffl F. 2002. Heat stress- and heat
shock transcription factor-dependent expression and activity of
ascorbate peroxidase in Arabidopsis. Plant Physiology 129,
Peltier G, Cournac L. 2002. Chlororespiration. Annual Review of
Plant Biology 53, 523–550.
Pfannschmidt T, Milsson A, Allen JF. 1999. Photosynthetic control
of chloroplast gene expression. Nature 397, 625–628.
Pfannschmidt T, Allen JE, Oelmu ¨ller R. 2001a. Principles of
redox control in photosynthetic gene expression. Physiologia
Plantarum 112, 1–9.
Pfannschmidt T, Schu ¨tze K, Brost M, Oelmu ¨ller R. 2001b. A
novel mechanism of nuclear photosynthesis gene regulation
by redox signals from the chloroplast during photosystem stoi-
chiometry adjustment. Journal of Biological Chemistry 276,
Pfannschmidt T, Schu ¨tze K, Fey V, Sherameti I, Oelmu ¨ller R.
2003. Chloroplast redox control of nuclear gene expression—
a new class of plastid signals in interorganellar communication.
Antioxidants and Redox Signaling 5, 95–101.
Pursiheimo S, Mulo P, Rintamaki E, Aro EM. 2001. Coregulation
of light-harvesting complex II phosphorylation and lhcb mRNA
accumulation in winter rye. The Plant Journal 26, 317–327.
S,Jimenez A,Cleary SP,
Chloroplast redox regulation1461
Rao MV, Lee HI, Creelman RA, Raskin I, Mullet JE, Davis KR.
2000. Jasmonic acid signalling modulates ozone-induced hyper-
senitive cell death. The Plant Cell 12, 1633–1646.
Rizhsky L, Davletova S, Liang H, Mittler R. 2004. The zinc finger
protein Zat12 is required for cytosolic ascorbate peroxidase 1
expression during oxidative stress in Arabidopsis. Journal of
Biological Chemistry 279, 11736–11743.
Romano PGN, Horton P, Gray JE. 2004. The Arabidopsis cyclo-
philins gene family. Plant Physiology 134, 1268–1282.
Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW. 2001.
Impaired sucrose-induction mutants reveal the modulation of
sugar-inducible starch biosynthetic gene expression by abscisic
acid signalling. The Plant Journal 26, 421–433.
Rouhier N, Gelhaye E, Jacquot JP. 2004. Plant glutaredoxins: still
mysterious reducing systems. Cell and Molecular Life Science 61,
Rushton PJ, Somssich IE. 1998. Transcriptional control of plant
genes responsive to pathogens. Current Opinion in Plant Biology
Saradadevi K, Raghavendra AS. 1992. Dark respiration protects
phtosynthesis against photoinhibition in mesophyll protoplasts od
pea (Pisum sativum). Plant Physiology 99, 1232–1237.
Schafer FQ, Buettner GR. 2001. Redox environment of the cell as
viewed through the redox state of the glutathione disulfide/
glutathione couple. Free Radicals in Biology and Medicine 30,
Schindler U, Beckmann H, Cashmore AR. 1992. TGA1 and G-box
binding factors: two distinct classes of Arabidopsis leucine zipper
proteins compete for the G-box-like element TGACGTGG. The
Plant Cell 4, 1309–1319.
Schmidt M, Dehne S, Feierabend J. 2002. Post-transcriptional
mechanisms control catalase synthesis during ist light-induced
turnover in rye leaves through theavailability of thehemin cofactor
and reversible changes of the translation efficiency of mRNA. The
Plant Journal 31, 601–613.
Schu ¨rmann P. 2003. Redox signaling in the chloroplast: the
ferredoxin/thioredoxin system. Antioxidants and Redox Signaling
Scott IM, Clarke SM, Wood JE, Mur LAJ. 2004. Salicylate
accumulation inhibits growth at chilling temperature in Arabidop-
sis. Plant Physiology 135, 1040–1049.
Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular responses
to dehydration and low temperature: differences and cross-talk
between two stress signalling pathways. Current Opinion in Plant
Biology 3, 217–223.
Snyders S, Kohorn BD. 2001. Disruption of thylakoid-associated
kinase 1 leads to alteration of light harvesting in Arabidopsis.
Journal of Biological Chemistry 276, 32169–32176.
Staswick PE, Tiryaki I. 2004. The oxolipin signal jasmonic acid is
activated by an enzyme that conjugates it to isoleucine in
Arabidopsis. The Plant Cell 16, 2117–2127.
Staswick PE, Tiryaki I, Rowe ML. 2002. Jasmonate response locus
jar1 and several related Arabidopsis genes encode enzymes of the
firefly luciferase superfamily that show activity on jasmonic,
salicylic, and indole-3-acetic acids in an assay for adenylation.
The Plant Cell 14, 1405–1415.
Strand A˚. 2004. Plastid-to-nucleus signalling. Current Opinion in
Plant Biology 7, 621–625.
Strand A˚, Asami T, Alonso J, Ecker JR, Chory J. 2003.
Chloroplast to nucleus communication by accumulation of Mg-
protoporphyrin IX. Nature 421, 79–83.
Sullivan JA, Gray JC. 2002. Multiple plastid signals regulate the
expression of the pea plastocyanin gene in pea and transgenic
tobacco plants. The Plant Journal 32, 763–774.
Sun Y, Oberley LW. 1996. Redox regulation of transcriptional
activators. Free Radicals in Biology and Medicine 21, 335–348.
Susek RE, Ausubel FM, Chory J. 1993. Signal transduction
mutants of Arabidopsis uncouple nuclear CAB and RBCS gene
expression from chloroplast development. Cell 74, 787–799.
Taylor WC. 1989. Regulatory interactions between nuclear and
plastid genomes. Annual Review of Plant Physiology and Plant
Molecular Biology 40, 211–233.
Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S,
Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M,
Inze ´ D, Van Breusegem F. 2004. Catalase deficiency drastically
affects gene expression induced by high light in Arabidopsis
thaliana. The Plant Journal 39, 45–58.
Vothknecht UC, Kannangara CG, von Wettstein D. 1998. Barley
glutamyl tRNAGLUreductase: mutations affecting haem inhibition
and enzyme activity. Phytochemistry 47, 513–519.
Weatherwax SC, Ong MS, Degenhardt J, Bray EA, Tobin EM.
1996. The interaction of light and abscisic acid in the regulation of
plant gene expression. Plant Physiology 111, 363–370.
Willekens H, Chamnongpol S, Davey M, Schraudner M,
Langebartels C, Van Montagu M, Inze ´ D, Van Camp W.
1997. Catalase is a sink for H2O2and is indispensable for stress
defense in C3plants. The EMBO Jounal 16, 4806–4816.
Wood ZA, Schro ¨der E, Harris JR, Poole LB. 2003. Structure,
mechanism and regulation of peroxiredoxins. Trends in Biochem-
ical Sciences 28, 32–40.
Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG. 1998.
COI1: an Arabidopsis gene required for jasmonate-regulated
defense and fertility. Science 280, 1091–1094.
Yabuta Y, Murata T, Yoshimura K, Ishikawa T, Shigeoka S.
2004. Two distinct redox signalling pathways for cytosoloc APX
induction under photo-oxidative stress. Plant Cell Physiology 45,
Yeh CM, Hsiao LJ, Huang HJ. 2004. Cadmium activates a
mitogen-activated protein kinase gene and MBP kinases in rice.
Plant and Cell Physiology 45, 1306–1312.
Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S. 2000. Expres-
sion of spinach ascorbate peroxidase isoenzymes in response to
oxidative stress. Plant Physiology 123, 223–233.
Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA.
1999. The Q0 site of cytochrome b6f complexes controls the
activation of LHCII kinase. EMBO Journal 18, 2961–2969.
1462 Baier and Dietz