properties necessary for photosynthesis, a process that con-
verts light energy into chemical energy. Changes in environ-
mental parameters such as light intensity, light quality, or
temperature affect the photosynthetic electron transport and
subsequently change the efficiency of light energy fixation.
Photosynthetic organisms therefore developed several mech-
anisms to acclimate to a wide range of environmental condi-
tions and to maintain the photosynthetic efficiency as high as
possible (2, 4, 20).
The light-driven chemistry of photosynthesis involves a se-
ries of redox steps in structural components or functionally
coupled pools of redox-active compounds, such as thiore-
doxin or glutathione. An increasing number of reports show
HLOROPLASTS, THE TYPICAL ORGANELLES of higher plants
and green algae, provide all structural and functional
that environmentally induced changes in the redox state of
these electron transport components act as signals that regu-
late the expression of proteins of the photosynthetic machin-
ery (for reviews, see 3, 9, 26, 42). This feedback mechanism
couples the present function of photosynthesis to the expres-
sion of its structural constituents and thus acclimates photo-
synthesis to changing environmental cues. As the photosyn-
thetic machinery consists of both plastid and nuclear encoded
products, this requires a high coordination in the expression
of these genes. Chloroplast redox signals play an important
role in this intracellular coordination; their impact on differ-
ent levels of plastid gene expression is also reviewed in this
issue. This review focuses on the role of chloroplast redox
signals in nuclear gene expression. It summarizes the present
knowledge about such pathways and describes the interaction
with other signaling cascades, as well as specific problems in
the transduction of these signals.
Institute of General Botany, Department of Plant Physiology, University of Jena, Jena, Germany.
Chloroplast Redox Control of Nuclear Gene Expression—A
New Class of Plastid Signals in Interorganellar Communication
THOMAS PFANNSCHMIDT, KATIA SCHÜTZE, VIDAL FEY,
IRENA SHERAMETI, and RALF OELMÜLLER
Chloroplasts are genetically semiautonomous organelles that contain their own subset of 100–120 genes cod-
ing for chloroplast proteins, tRNAs, and rRNAs. However, the great majority of the chloroplast proteins are
encoded in the nucleus and must be imported into the organelle after their translation in the cytosol. This
arrangement requires a high degree of coordination between the gene expression machineries in chloroplasts
and nucleus, which is achieved by a permanent exchange of information between both compartments. The ex-
istence of such coordinating signals has long been known; however, the underlying molecular mechanisms
and signaling routes are not understood. The present data indicate that the expression of nuclear-encoded
chloroplast proteins is coupled to the functional state of the chloroplasts. Photosynthesis, which is the major
function of chloroplasts, plays a crucial role in this context. Changes in the reduction/oxidation (redox) state
of components of the photosynthetic machinery act as signals, which regulate the expression of chloroplast
proteins in both chloroplasts and nucleus and help to coordinate the expression both in compartments. Recent
advances in understanding chloroplast redox regulation of nuclear gene expression are summarized, and the
importance for intracellular signaling is discussed. Antioxid. Redox Signal. 5, 95–101.
ANTIOXIDANTS & REDOX SIGNALING
Volume 5, Number 1, 2003
© Mary Ann Liebert, Inc.
13214c12.pgs 2/14/03 2:52 PM Page 95
NUCLEAR GENE EXPRESSION—
ATARGET FOR CHLOROPLAST
Light regulation of nuclear gene expression is an exten-
sively investigated field of research in plant biology, and the
impact of photoreceptor-controlled signaling cascades is well
documented (for reviews, see in 1, 5, 14, 16, 25, 33, 47).
Chloroplast redox control, however, is a new concept of how
light can influence the expression of nuclear genes. By this
way, photosynthesis contributes important information to the
regulation of nuclear gene expression that is not sensed by
cytosolic photoreceptors. Through this, the chloroplast serves
as a sensor for environmental changes and can induce physio-
logical acclimation reactions (Fig. 1). The activation of tran-
scription of nuclear encoded photosynthesis genes by illumi-
nation is a long-known phenomenon, but the first clear
evidence that such regulation can be coupled to photosyn-
thetic electron transport came from studies with the unicellu-
lar algae Dunaliella tertiolecta and Dunaliella salina (17, 28).
Escoubas et al. (17) demonstrated that transcription of the
Lhcb genes [encoding chlorophyll-binding proteins of light-
harvesting complex II (LHCII)] is stimulated when high
light-acclimated cells are exposed to low-light intensities. By
performing the same experiments in the presence of the site-
specific electron transport inhibitors 3-(3?,4?-dichloro-
phenyl)-1,1?-dimethylurea (DCMU) and 2,5-dibromo-3-
methyl-6-isopropyl-p-benzoquinone (DBMIB) (51), they
could show that this increase is coupled to photosynthetic
electron transport. In addition, they identified the redox state
of the plastoquinone pool (PQ) as the controlling parameter:
an oxidized PQ pool (generated by low light or DCMU treat-
ment) activates Lhcb transcription, whereas a reduced one
(generated by high light or DBMIB treatment) represses it.
In an independent study, Maxwell et al. (28) came to simi-
lar conclusions. They analyzed Lhcb transcription and LHCII
apoprotein content in response to varying light intensities
under controlled temperature environments. This approach is
based on the observation that light-intensity effects also de-
pend on ambient temperature. For instance, the same light
intensity that represents low-light condition at a high tem-
perature can also represent high-light condition under low
temperature. The enzymatic steps in the photosynthetic dark
reaction become rate-limiting under low temperature, thus
generating a higher excitation pressure. In their experiments,
Maxwell et al. (28) found that relaxation of high excitation
pressure both thermodynamically (shifting cells from 13°C to
30°C under constant light) and photodynamically (shifting
cells from light to dark growth regimes under constant tem-
perature) results in an increase of Lhcb transcription and
LHCII protein accumulation. They concluded that the redox
poise of intersystem electron transport represents a common
sensing/signaling pathway for Lhcb transcription under vari-
ous stress conditions.
A recent study using Lemna perpusilla as model organism
demonstrated that Lhcb transcript abundance and LHCII pro-
tein content are increased under low-light intensities also in a
higher plant (52). Using a cytochrome b6f complex (cyt b6f)
deficient mutant, Yang et al. (52) showed that this regulation
is coupled to photosynthetic electron transport. The mutant
failed to respond to changing light intensities and exhibited
always a high light-acclimated phenotype. Further investiga-
tions with DCMU in combination with results from the pho-
tosynthetic mutant led to the conclusion that the redox state
of the PQ pool represents the controlling redox parameter in
this regulation, which is fully consistent with the observa-
tions described above.
High-light treatment was also used to demonstrate the exis-
tence of another type of chloroplast redox signals in the
higher plant Arabidopsis thaliana (22). An increase of inci-
dent light intensity from 200 to 2,000 µE increased the tran-
script level of two genes for cytosolic ascorbate peroxidases
(Apx1, Apx2) within 15 min. DCMU and DBMIB treatments
96 PFANNSCHMIDT ETAL.
tion, result in changes of photosynthetic efficiency. Concomitantly, the redox state of chloroplast components is affected. Such
redox changes represent a sensor for the environmental fluctuation and serve as signals that influence the expression of nuclear
genes whose products, in turn, are involved in an appropriate physiological response to counteract the limitation of photosynthe-
sis by the environment. A general scheme for this is given at the top of the figure; several concrete examples are summarized
below. For more details, see text.
Physiological role of chloroplast redox signals. Fluctuating environmental conditions, especially changes in illumina-
13214c12.pgs 2/14/03 2:52 PM Page 96
of leaf discs indicated that this signaling pathway originates
from the PQ pool; however addition of reduced glutathione
abolished this signal, suggesting that the redox state of the
glutathione pool may play an interacting regulatory role in
this context. Both ascorbate peroxidases and glutathione are
scavengers of reactive oxygen species (ROS) that are gener-
ated preferentially under stress conditions, such as high light.
Further experiments with transgenic Arabidopsis plants con-
taining Apx2 promoter:luciferase fusions demonstrated that
the high light-induced signal can be transported from a high
light-treated tissue to an untreated tissue plant probably via
high light-generated hydrogen peroxide (H2O2) (23). This
phenomenon, called “systemic acquired acclimation,” sug-
gests that redox signals in higher plants not only are trans-
duced from chloroplasts to the nucleus of the same cell, but
also function in a tissue overriding manner. Further inves-
tigations demonstrated that also transcripts for a peroxiso-
mal catalase (Cat2), the chloroplast glutathione peroxidase
(Gpx2), and glutathione S-transferase (Gst), as well as the
pathogenesis-related type 2 protein (Pr2), were induced by
light stress, but interestingly only in systemic, nonilluminated
In transgenic tobacco plants harboring a pea ferredoxin
transcribed region (Fed1) under the control of the cauliflower
35S promoter, the abundance of this Fed1 message was four-
to fivefold increased in reilluminated plants compared with
dark-adapted plants (38). The light-induced increase was
shown to be coupled to photosynthetic electron transport be-
cause DCMU treatment could abolish the light effect. This re-
sponse is gene-specific because Lhcb transcript accumulation
was not affected by the drug. In addition, it could be demon-
strated that light-dependent polyribosome loading of Fed1
mRNA, an important prerequisite for efficient translation,
was also diminished by the DCMU treatment. The same was
observed for the Lhcb message. Further experiments indi-
cated that interruption of photosynthetic electron transport by
either dark or DCMU treatment led to a rapid destabilization
of the Fed1 mRNA (39). Taken together, these observations
demonstrate that chloroplast redox signals affect also post-
transcriptional events besides transcription.
In mustard photosystem stoichiometry adjustment in re-
sponse to varying light-quality conditions was shown to be
regulated by PQ redox control of transcription of the chloro-
plast genes psbA and psaAB [encoding reaction center
proteins of photosystem II (PSII) and photosystem I (PSI)]
(41). In a recent study using transgenic tobacco plants har-
boring promoters of nuclear-encoded PSI genes petE, petH,
psaD, and psaF [encoding plastocyanin (PC), the ferre-
doxin:NADP:oxidoreductase (FNR), and the PSI subunits
PsaD and PsaF] fused to the uidA gene, it could be demon-
strated that the same light-quality variations also affect nu-
clear gene expression (43). In combination with DCMU and
DBMIB treatments, these experiments showed that the PC
promoter activity is controlled by the redox state of the PQ
pool, whereas the psaD and psaF promoters are under the
control of a yet unidentified downstream component of the
photosynthetic electron transport chain. All three promoters
have in common that they are activated by the reduction of
photosynthetic electron transport components. The FNR pro-
moter revealed no regulation under any condition. A further
study using the same experimental approach showed that the
Arabidopsis nitrate reductase (Nia2) promoter also responds
to the light-induced redox signals. However, it is activated by
a predominant oxidation of the electron transport components
either by PSI light or by DCMU or DBMIB treatment (45).
Beside transcription, the nitrate reductase enzyme activity
was regulated in exactly the same way. The use of a cyt b6f-
deficient Lemna aequinoctialis mutant (8) confirmed that the
photosynthetic electron transport regulates nitrate reductase
activity. The mutant showed constitutive high activity under
all conditions similar to PSI light-acclimated wild type.
These results show that redox signals that are shown to act
within the organelle (41) can also extend to the nucleus and
that the same signal can have different gene-specific effects.
These examples show that chloroplast redox signals affect
nuclear gene expression under various physiological condi-
tions and at different levels of expression. The increasing
number of reports describing such regulation pathways sug-
gests that a complex network of redox signals rather than a
single signaling pathway couples chloroplast function to the
nuclear gene expression machinery.
INTERACTION OF REDOX SIGNALS WITH
OTHER SIGNALING PATHWAYS
All chloroplast redox signals described in the previous
section are connected to illumination and photosynthesis. As
photosynthesis is the central point of plant energy metabo-
lism that is connected with almost all processes in the cell, it
should be expected that there exist interactions with other
regulating signals (Fig. 2). An example for this can be found
in a recent study with an Arabidopsis cell culture (36). It is
well known that high external sugar concentrations repress
nuclear photosystem gene expression (46). Oswald et al. (36)
found that the increase in transcription of Lhcb and RbcS
genes, which is normally observed when the external sugar is
removed, can be blocked by addition of DCMU to the culture
medium. The same experiments performed with transgenic
Arabidopsis lines carrying Lhcb2 and PC promoters fused to
CHLOROPLAST REDOX SIGNALS REGULATE NUCLEAR GENES97
signals with other signaling pathways during control of nu-
clear gene expression. Thick arrows indicate redox signals;
thin arrows are influences of various parameters on cellular
components or processes. Black circles indicate interactions of
signaling pathways. CP, chloroplast. For more details, see text.
Known and putative interactions of plastid redox
13214c12.pgs 2/14/03 2:52 PM Page 97
the luciferase reporter gene confirmed these results in planta.
Further investigations using the sugar-insensitive Arabidopsis
mutant sun6 also carrying the PC-LUC construct revealed
that the PC promoter activity is increased by sugars and that
DCMU treatment has no effect on this response. Oswald et al.
(36) postulated that under weak light a redox signal from
photosynthetic electron transport activates the derepression
of nuclear photosynthetic genes when the strong antagonistic
suppression by external sugars is removed. This signal is not
active once derepression has occurred. This suggests that
photosynthetic gene expression is balanced by cellular sugar
status and photosynthetic activity to fulfil the demands of en-
ergy metabolism. If this model also accounts for high-light
conditions has to be tested.
As described above, excess-light-induced ROS formation
activates nuclear antioxidant genes (22); however, the genera-
tion of ROS can be also observed under other abiotic or biotic
stresses, such as chilling, wounding, or pathogen attack. It
has been shown that transcripts for several components of the
cytosolic ROS-scavenging system are induced by such
stresses (for review, see 31). ROS formation also affects the
degree of reduction of major antioxidant pools, such as glu-
tathione, which is regarded as a key component of antioxidant
defense in plants (18). In general, there is increasing evidence
that ROS and the redox states of antioxidant pools regulate
the expression of nuclear antioxidant genes. In this instance,
redox signals via ROS serve as integrating components of
several signaling pathways that help the plant to adapt to var-
ious types of stresses. As the cell is not able to identify the re-
spective type of stress only by recognizing the ROS levels in
the stroma of the plastid or in the cytoplasm, further signals
are required. For instance, in the case of systemic acquired re-
sistance, ROS provide the common signal for stress, but the
response appears to be elicited only in co-action with nitric
oxide (13). Therefore, ROS-mediated redox signals may inter-
act with many other signals to define changes in environmen-
tal conditions. The importance for a sensitive sensing of cellu-
lar ROS levels has been demonstrated also in transgenic
tobacco plants overexpressing a plastid ?-glutamylcysteine
synthetase. Despite the potentially higher ROS scavenging ca-
pacity, these plants suffered from strong oxidative stress that is
caused most probably by their inability to sense changes in
ROS formation (12).
Redox signals induced by the photosynthetic process are
strictly light-dependent. From the present data, it appears that
different types of signals can be generated depending on the
incident-light quantity, and a model has been proposed in
which such different signals operate in a hierarchical order
(42). It appears likely that under certain conditions, different
redox-controlled signaling pathways may interact with each
Light-regulated nuclear gene expression is largely affected
by the red and blue light-absorbing cytosolic photoreceptors
(see Introduction). Furthermore, there exists increasing evi-
dence that plastid signals interact with phytochrome signal-
ing pathways that also influence expression of nuclear genes
for plastid proteins (27). At present, it is unclear if chloro-
plast redox signals interfere or interact with cytosolic pho-
toreceptor cascades. The availability of photoreceptor mu-
tants provides a useful tool to solve this problem. First results
show that phytochrome A- and phytochrome B-deficient Ara-
bidopsis mutants respond in the same way to light quality-
induced redox signals as the wild type, which indicates that
the redox signaling cascade is functional in phytochrome A-
and phytochrome B-deficient Arabidopsis mutants (Fey and
Pfannschmidt, unpublished observations).
CHLOROPLAST REDOX SIGNALS AND
THEIR ROLE AS “PLASTID FACTOR”
Early investigations in the 1980s especially with norflura-
zon, an inhibitor of phytoene desaturase, gave the first hints
that chloroplast function or development influences nuclear
gene expression. This led to the postulation of a so-called
“plastid factor” that couples the functional state of the plas-
tids to the expression of nuclear encoded plastid proteins (for
reviews, see 34, 50). Norflurazon-treated plants exhibit a
white phenotype that is caused by an arrest in chloroplast bio-
genesis through photobleaching because the inhibitor blocks
chlorophyll biosynthesis. As a concomitant effect, an inhibi-
tion of the expression of some nuclear genes (i.e., RbcS,
Lhcb) encoding chloroplast proteins was observed. The same
results were obtained when chloroplast gene expression was
blocked by inhibitors such as tagetitoxin, rifampicin, or cylo-
heximide (for review, see 19), suggesting the involvement of
(a) chloroplast gene product(s) in this retrograde signaling.
Further studies point to intermediates or enzymatic compo-
nents of the chlorophyll biosynthesis pathway as putative
plastid regulators of nuclear gene expression (for reviews, see
6, 21, 37, 44).
The molecular nature of the “plastid factor(s),” as well as
the way this signal is transduced across the chloroplast enve-
lope into the cytosol, is still unknown. Recent studies with
Arabidopsis cue1, gun5, and laf6 mutants, however, have
shed more light on this complex signaling network. Their de-
fects are located in the phosphoenolpyruvate/phosphate
translocator (cue1), the H subunit of the magnesium chelatase
(gun5), and a new ABC transporter protein (laf6). All three
components are located in the chloroplast envelope, suggest-
ing that the defect interrupts the transport of one or several
plastid factor(s), and models of respective signaling pathways
have been proposed (29, 30, 48). Earlier studies with mustard
(35, 40) and a recent study on the pea lip1 mutant (49), which
shows photomorphogenic development in the dark, demon-
strated that nuclear photosynthesis gene expression depends
on plastid translation or transcription in a light-independent
manner. This suggests that the plastid factor(s) is not neces-
sarily coupled to light, thylakoid formation, or photosyn-
thesis. At present, it is not clear how this light-independent
signal relates to the signaling pathways identified in the Ara-
bidopsis mutants; however, as redox signals from photosyn-
thesis are strictly light-dependent, they represent a different
class of plastid signals.
Mutants with defects in chloroplast-to-nucleus signaling
often show strong developmental defects (19, 44). Especially
in the beginning of cell or tissue differentiation, the develop-
mental state of plastids may be a very important parameter
for further development of its host cell. Early plastid signals
98 PFANNSCHMIDT ETAL.
13214c12.pgs 2/14/03 2:52 PM Page 98
therefore may represent light-independent developmental sig-
nals, whereas plastid signals in fully developed tissue report
the actual physiological state of the organelle. From the pres-
ent data, it is apparent that photosynthetic redox signals play
an important role in this second class of signals (compare
Fig. 1). In addition, it can be assumed that cytosolic photore-
ceptors may play an important role in gene expression control
of plastid proteins during greening of seedlings and that its
role is overtaken by other factors such as chloroplast redox
signals in fully green plants.
Although the function of chloroplast redox signals appears
to be relatively clear, the molecular mechanisms of its trans-
duction toward the nucleus are only poorly understood
(Fig. 3). Best models for signal transduction exist for H2O2–
mediated redox signals. H2O2is known to be membrane-
permeable and may pass the chloroplast envelope without
directed transport. In the cytosol it induces the respective
change in gene expression by activating a mitogen-activated
protein kinase cascade (24). For redox signals starting from
the PQ pool, the transduction is less clear. It is likely that the
same signaling pathway that regulates the state transition also
regulates chloroplast gene expression (3), and it is conceiv-
able that an additional branch of this pathway extends to the
nucleus. How the signal passes the envelope, for instance via
a transporter, is unknown to date. However, there exists ex-
perimental evidence that the PQ redox signal is transformed
into a phosphorylation signal in the cytosol (10, 17). As a sec-
ond possibility, PQ redox signals may be sent directly to the
nucleus via PQ molecules located in the envelope membrane.
As the inner-chloroplast membrane system is in close contact
to the envelope and envelope-located electron transport has
been found (32), such PQ molecules could report the redox
state of the PQ pool to a putative cytosolic receptor. Chloro-
plast redox signals may be also reported to the nucleus indi-
rectly by their effects on chloroplast gene expression or by af-
fecting the biochemistry of the organelle. As outlined above,
there exist plastid signals that tightly couple nuclear gene ex-
pression to the function of chloroplast gene expression and
therefore to inner-chloroplast redox signals. Besides these
possible transduction pathways, several redox-regulated gene
expression events are described from which the transduction
of the redox signals is completely unknown.
CHLOROPLAST REDOX SIGNALS REGULATE NUCLEAR GENES99
redox signals to the nucleus. Photosynthetic electron trans-
port components are sketched within a chloroplast (CP). Hori-
zontal lines above them represent the thylakoid membrane sys-
tem and indicate its connection with the envelope of the
chloroplast. Arrows represent redox signals; dotted arrows rep-
resent putative redox signaling pathways. MAPK, mitogen-
activated protein kinase. For details, see text.
Putative transduction mechanisms of chloroplast
TABLE 1.SUMMARY OF REDOX-CONTROLLED NUCLEAR GENES SORTED BY TYPE OF REGULATING REDOX SIGNAL
Activating redox control parameter
Oxidation signalsGene and gene class* Organism and reference
Apx1, Apx2 (AOS)
Oxidized PQ pool
Oxidized intersystem electron carrier
Oxidized PQ pool
Reduced PQ pool, high H2O2 concentration
Dunaliella tertiolecta (17)
Dunaliella salina (28)
Lemna perpusilla (52)
(transgenic) (22, 23)
Arabidopsis (cell culture) (36)
Tobacco (transgenic) (45)
Gpx2, Cat2, Gst, Pr2 (AOS)
Lhcb2, RbcS (PSY)
Photosynthetic electron transport (oxidized)
Photosynthetic electron transport (oxidized)
PsaD, PsaF (PS)
Photosynthetic electron transport (reduced)
Photosynthetic electron transport (reduced)
Reduced PQ pool
Photosynthetic electron transport (reduced)
Tobacco (transgenic) (38)
Arabidopsis (transgenic) (36)
Tobacco (transgenic) (43)
Tobacco (transgenic) (43)
*For physiological details and encoded proteins, see text. LH, light-harvesting genes; AOS, antioxidant and stress genes; M,
metabolic genes; PSY, photosynthesis genes; PS, photosystem genes.
13214c12.pgs 2/14/03 2:52 PM Page 99
The increasing number of reports describing chloroplast
redox control of nuclear gene expression suggests that there
exist more signals than previously anticipated and underlines
the importance of such signals for the development and me-
tabolism of the cell. Currently, we have more questions than
answers; however, the present data already show that redox
signals are involved in many signaling pathways, such as
light, stress, energy, and metabolic signaling, and more are
expected. In addition, redox signals from other cell compo-
nents, i.e., mitochondria and peroxisomes (for review, see
11), may interact with those from the chloroplast. Further-
more, the identity and number of all redox-controlled genes
are unknown to date. Genomic approaches using microarray
techniques will give us a more complete picture within the
next few years. A first study using a H2O2-treated Arabidopsis
cell culture showed that at least 175 different open reading
frames responded to oxidative stress (15). As the number and
identities of redox-responsive genes will vary depending on
the physiological test systems, the presently known genes
(Table 1) may represent only the tip of the iceberg. It will be
fascinating work to unravel all the roles that redox signals
play in the intracellular signaling network.
Work in the authors’ laboratories is supported by the
cyt b6f, cytochrome b6f complex; DBMIB, 2,5-dibromo-
dichlorophenyl)-1,1´-dimethylurea; FNR, ferredoxin:NADP:
oxidoreductase; H2O2, hydrogen peroxide; LHCII, light-
harvesting complex of photosystem II; PC, plastocyanin; PQ,
plastoquinone; PSI, photosystem I; PSII, photosystem II;
ROS, reactive oxygen species.
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Received for publication November 1, 2001; accepted January
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