Download Efficient high light acclimation involves rapid

Journal of Experimental Botany, Vol. 66, No. 9 pp. 2401–2414, 2015
doi:10.1093/jxb/eru505 Advance Access publication 7 January 2015
REVIEW PAPER
Efficient high light acclimation involves rapid processes at
multiple mechanistic levels
Karl-Josef Dietz*
Biochemistry and Physiology of Plants, Faculty of Biology, W5-134, Bielefeld University, University Street 25, 33501 Bielefeld, Germany
* To whom correspondence should be addressed. E-mail: [email protected]
Received 10 October 2014; Revised 19 November 2014; Accepted 24 November 2014
Abstract
Like no other chemical or physical parameter, the natural light environment of plants changes with high speed and
jumps of enormous intensity. To cope with this variability, photosynthetic organisms have evolved sensing and
response mechanisms that allow efficient acclimation. Most signals originate from the chloroplast itself. In addition to very fast photochemical regulation, intensive molecular communication is realized within the photosynthesizing cell, optimizing the acclimation process. Current research has opened up new perspectives on plausible but
mostly unexpected complexity in signalling events, crosstalk, and process adjustments. Within seconds and minutes,
redox states, levels of reactive oxygen species, metabolites, and hormones change and transmit information to the
cytosol, modifying metabolic activity, gene expression, translation activity, and alternative splicing events. Signalling
pathways on an intermediate time scale of several minutes to a few hours pave the way for long-term acclimation.
Thereby, a new steady state of the transcriptome, proteome, and metabolism is realized within rather short time periods irrespective of the previous acclimation history to shade or sun conditions. This review provides a time line of
events during six hours in the ‘stressful’ life of a plant.
Key words: Cell signalling, gene expression, light acclimation, metabolites, photosynthesis, redox regulation, translation.
Necessity for light acclimation
Light acclimation may be considered a prototypic environmentally induced process in which chloroplast and extrachloroplast activities are adjusted in a coordinated manner
in order to optimize metabolism and maximize overall fitness, but also to avoid damage (Spetea et al., 2014). Fitness
is defined as the production of a high biomass and many
seeds, while damage (decreasing fitness) can be measured
at the level of, for example, oxidized proteins. Acclimation
describes all processes that are altered in the plant in order
to cope with the changing environment. It is achieved by the
plant sensing the environmental change and activating the
appropriate molecular programme. As long as acclimation
is not realized, the plants may encounter stress, i.e. a major
deviation from optimal conditions. Like no other type of
metabolism, photosynthesis switches almost instantaneously
from very high to very low rates if photon flux densities
suddenly drop or increase, e.g. in response to moving sun
flecks in understorey vegetation. On the one hand, photon
flux density in full sunlight exceeds the energy input exploitable by metabolism. Consequently, excessively absorbed
energy must be dissipated safely. On the other hand, in dim
light, energy conversion should proceed with the highest
efficiency possible to maximally exploit the limiting energy
input. Considering the ease with which the quantity of light
can be manipulated, it is unsurprising that light shifts have
been widely used for decades by experimentalists exploring
the mechanisms of coordination and regulation involved.
Likewise, long-term structural and physiological acclimation and genomic adaptation have been explored for many
years. The latter mechanisms are not the topic of this review.
© The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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2402 | Dietz
Light acclimation research in a historical
perspective
Early interest in light acclimation focused on reorganization
of plant structure, organ properties, and chloroplast ultrastructure (Boardman, 1977). Different short- and long-term
processes interfere with light harvesting. On a subcellular
scale, stacking of grana increases in shade-acclimated leaves.
Single-turnover flashes allowed the chlorophyll cross section
which supplies energy to each photosynthetic reaction centre
to be defined. The number of chlorophyll molecules per photosystem II (PSII) reaction centre (the so-called photosynthetic units) ranged between 220 and 480 in eight sun species,
and 630 to 940 in six shade species (Malkin and Fork, 1981).
By this mechanism light harvesting is optimized in low lightacclimated leaves such that more chlorophyll molecules serve
fewer reaction centres. This minimizes resource investments
in the build-up of reaction centres that only receive limited
energy at low light intensities. Such a light-harvesting efficient photosynthetic apparatus would be prone to damage by
excess light as soon as the light climate changes. Nevertheless
in such low light-acclimated leaves, the photosynthetic electron transport chain (PET) can immediately be reorganized
in response to excessively absorbed light. Several mechanisms
allow for energy dissipation to heat (non-photochemical
quenching, NPQ). Such mechanisms allow plants rapidly to
cope with variations in the quality and quantity of light that
frequently occur in nature (Ruban et al., 2007). Since NPQ in
light-harvesting antennae is unlikely to account for all photoprotection processes, reaction centre quenching also needs
to be considered (Weis and Berry, 1987; Sane et al., 2012).
In addition to such short-term light acclimation involving
biochemical regulation, long-term acclimation ‘tunes’ the
stoichiometry of photosynthetic components (Puthiyaveetil
et al., 2012), activity of metabolic pathways and antioxidant
defence, and thylakoid structure predominantly by modifying nuclear gene expression (Pfannschmidt et al., 2010). The
suitability of photosystems as environmental sensors was discussed by Anderson et al. (1995), who stressed the idea of the
‘grand design’ of photosynthesis which links the performance
of photosynthesis to signalling and acclimation.
Dissecting the time frame of PET-linked responses, energydependent quenching (qE) operates within seconds of an
increase in light (Öquist et al., 1992). Acidification of the thylakoid lumen indicates proton accumulation by water-splitting activity and the plastoquinone shuttle in excess of the
use of proton motive force in ATP synthesis and activates the
xanthophyll cycle. Incorporation of zeaxanthin into the lightharvesting complexes fosters dissipation of absorbed energy
as heat (Demmig et al., 1987). Changes in the ratio of linear to
cyclic electron transport are also rapidly induced (Shikanai,
2014). State transitions which represent the reorganization of
light-harvesting antennae between PSI and PSII occurs on a
slightly longer time scale of minutes and is referred to as qT
(Puthiyaveetil et al., 2012). Quenching through photoinhibition which involves disassembly and repair of PSII is named
qI and occurs on a scale of hours (Aro et al., 2005). The latter
mechanism also involves adjustment of gene expression. If
the reduction state of the chloroplast increases, plastid terminal oxidase (PTOX) and mitochondrial alternative oxidase
(AOX) also offer mechanisms for dissipating excess reducing
energy (McDonald et al., 2011; Ivanov et al., 2012).
In parallel to photochemical adjustment, activation of carbon metabolism, in particular the Calvin cycle, occurs in a
feed-forward manner through alkalization of the stroma, and
an increase in Mg2+ concentration and reduction power, in
particular by thiol-dependent activation of critical components such as the γ-subunit of the ATP synthase and enzymes
such as fructose-1,6-bisphosphatase. Thioredoxins and lessexplored glutaredoxins play a crucial in thiol redox-related
regulation (Nikkanen and Rintamäki, 2014). Many chloroplast proteins have been identified as targets of reversible
redox regulation by e.g. thiol-disulfide transitions, glutathionylation, intermolecular disulfide bonding, S-oxygenation,
and S-nitrosylation (Buchanan and Balmer, 2004; König
et al., 2012; Michelet et al., 2013). These principles have been
known for quite some time, but new targets and regulators are
still being discovered. Previously such regulatory mechanisms
were considered to be unique and specific to a few processes,
but they have now emerged as central components which are
used in the local and retrograde signalling network of light
acclimation.
Chloroplast to nucleus signalling as a
critical component of acclimation
Retrograde signalling from the chloroplast to the nucleus in
photosynthesizing leaves has been termed ‘operational control’, which is distinguished from signal transduction components exclusively active during seedling and leaf development
(‘biogenic control’) (Pogson et al., 2008). The classification
as operational control can be further refined, e.g. by distinguishing signals in metabolic regulation, stress acclimation,
and cell death induction. In addition to information exchange
between plastids and the nucleus, the mitochondrion is now
being recognized as an equally important player in anterograde and retrograde control of the three genetic compartments of plant cells (Schwarzländer and Finkemeier, 2013)
(Fig. 1). In addition photosynthesis rapidly alters metabolism
in other compartments, such as peroxisomes, which then also
contribute to retrograde signalling, e.g. by redox and reactive
nitrogen species (del Rio et al., 2003). Importantly, with few
exceptions, eukaryotic cells have only one nucleus but hundreds of organelles. Thus, the nucleus responds in some sort
of averaged manner to multiple retrograde signals originating from many organelles (Pfannschmidt, 2010). It may be
assumed that chloroplast metabolism in a cell is inhomogeneous. Let us consider a leaf palisade cell. There are chloroplasts that are located near the upper sun-exposed epidermis.
They experience higher light intensities than chloroplasts in
the part of the cell which is in the ‘most interior’ part of the
leaf. This is an underexplored topic (Lepistö et al., 2012).
Concepts should be developed which deal with the impact
of retrograde signals released from chloroplasts in the vicinity of the nucleus. It appears reasonable to assume that their
Timeline of light acclimation | 2403
influence on nuclear gene expression is larger than that of distant chloroplasts.
Altered electron pressure in the PET is among the immediate biochemical changes encountered upon changes in light
intensity. Thus redox signals originating from photosynthetic
electron transport are important regulators of short-term
and long-term acclimation (Escoubas et al., 1995; Fey et al.,
2005) (Fig. 2). Other players in retrograde signalling are redox
cues generated downstream of PSI, e.g. linked to NADPH or
thioredoxin (Baier et al., 2005; Bräutigam et al., 2009); abscisic acid (ABA) synthesized from carotenoids in the thylakoid
Fig. 1. Involvement of organelles in photosynthesis-related retrograde
signalling. Light signalling that affects light acclimation is here defined as
photosynthetically active radiation and originates from chloroplasts, but
indirectly also from other metabolically tightly interlinked organelles like
mitochondria and peroxisomes. All emitted signals are integrated in the
cytosol and then act on nuclear gene expression. Thus crosstalk and
signal integration is already realized at the level of organelles.
membrane (Galvez-Valdivieso et al., 2009); metabolites and
end products such as sugars; chlorophyll ana- and catabolites
(Papenbrock et al., 2001; Pruzinská et al., 2003;); reactive
oxygen species (ROS) including 1O2 and H2O2 (Meskauskiene
et al., 2001; op den Camp et al., 2003), glutathione, and ascorbate; and ROS-dependent lipid peroxide degradation and
processing products including jasmonic acid (JA) (Müller and
Berger, 2009), salicylic acid (SA), and ethylene linked to ROS
(Mateo et al., 2006). This order of signals tentatively coincides with the degree of metabolic imbalance encountered by
photosynthetic leaves and needed to elicit them. Signalling
linked to organellar gene expression shows overlap with lightand cold-stress signalling pathways. In addition there appears
to be a connection with the endoplasmic reticulum (ER)
and ER-residing transcription factors (Leister et al., 2014).
Figure 3 sorts these retrograde signals into the framework
of environmentally induced metabolic adjustment, stress
acclimation, and cell death induction. For the time being,
JA, SA, ethylene, and ROS are linked to more severe stress.
The JA/ethylene and SA signalling pathways act antagonistically in plant responses to severe biotic and abiotic stresses
and function in combination with ROS in plant immunity
as well as in triggering cell death programmes (Tsuda et al.,
2009). The SA signalling pathway is involved in immunity to
biotrophs including bacterial pathogens like Pseudomonas
syringae, while JA and ethylene signalling affects immunity to
necrotrophs, e.g. the fungal pathogen Alternaria brassicicola
(Glazebrook, 2005). The immune response depends on the
development of controlled cell death. Lesion mimic mutants
which form necrotic spots on leaves serve as models for the
development of cell death. Lesion development in such
mutants, particularly in propagation mutants, often depends
on light (Meng et al., 2009). This suggests that chloroplast
processes affect or guide the response to severe biotic and
abiotic stress (Anderson et al., 1995; Pfannschmidt, 2003).
Cytosol/nucleus
Chloroplast
ascorbate, GSH
redox
DHAP
redox, energy, sugar
MDH
NADPH
Trx
e-
redox
thiol redox
O2-
↑O2
redox, NADPH
H2O2
redox, ROS
metabolites
C-, N- metabolites
ABA
ABA
oxylipins
OPDA
executer
signaling
chlorophyll
metabolites
signaling
Stn7
signaling
plastid translation
signaling
metabolites
hormones
signal transduction
poorly understood
pathways
Fig. 2. Categorization of retrograde signalling. The schematic summarizes signals and mechanisms which function as retrograde signals and affect
cytosolic/nuclear events. They are categorized in four groups: redox-, metabolite-, and hormone-linked mechanisms, and signals transmitted via signal
transduction chains which are mostly poorly understood. MDH, malate dehydrogenase; Stn7, a thylakoid associated protein kinase.
2404 | Dietz
Fig. 3. Functional assignment of retrograde signals to the regulatory
targets of metabolic adjustment, stress acclimation, and cell death. The
shading of green to red indicates increasing intensities. This may be
illustrated with the interchain reduction state. It is used to enable tuned
adjustment of complex assembly and light harvesting at low light, but
severe redox imbalance affects stress acclimation. On the other hand SA
interferes with cell death. PQ, plastoquinone.
In this way, the singlet oxygen pathway initially discovered
with the flu mutants (Meskauskiene et al., 2001) and refined
by the identification of suppressor mutants (Meskauskiene
et al., 2009) appears to take part in a cell death programme
under stress, but also possibly participates in retrograde signalling in operational control (Triantaphylidès and Havaux,
2009). 1O2 released in the flu mutant activates genes of the
JA pathway (op den Camp, 2003) and triggers cell death in
an executer-dependent manner (Kim et al., 2012) (Fig. 3). By
genetic analysis, Mühlenbock et al. (2008) assigned a linkage function to chloroplast signalling which enables mutual
crosstalk between light acclimation and plant immunity.
Anabolites and catabolites of tetrapyrrole synthesis appear
to function as signalling compounds under severe stress,
but may also exert operational control under conditions
of moderate metabolic imbalance. Mutants disturbed in
tetrapyrrole biosynthesis or degradation pathways frequently
exhibit spontaneous cell death phenotypes and often in a
light-dependent manner indicating their involvement in programmes of biotic stress defence (Schlicke et al., 2014). For
example, the accelerated cell death 1 gene in Arabidopsis thaliana is homologous to lethal leaf spot 1 (LLS1) of maize and
encodes the phaeophorbide a (pheide) oxygenase. The lls1
mutants in maize accumulate pheide and form light-dependent lesions (Pruzinská et al., 2003). Suppression of plastidic
ferrochelatase activity in tobacco by FeChI antisense RNA
expression reduced leaf chlorophyll content and elicited the
formation of necrotic leaf lesions in a light intensity-dependent manner (Papenbrock et al., 2001). GUN4 is involved in
regulating tetrapyrrole biosynthesis and participates in retrograde signalling (Brzezowski et al., 2014).
Mateo et al. (2006) established a role of SA in high light
acclimation and redox homeostasis of Arabidopsis using
mutants accumulating higher (cpr1-1, cpr5-1, cpr6-1, and
dnd1-1) or lower (nahG and sid2-2) SA levels than the wild
type. The dwarf-like phenotype of SA over-accumulators in
low light was overcome in high light, while high light acclimation was disturbed in low SA accumulators. In addition, the
amounts of H2O2 and glutathione correlated with the levels
of SA in tissue and high SA content enhanced catalase, Cu/
Zn-superoxide dismutase, and glutathione reductase activities (Mateo et al., 2006). The authors concluded that the tight
coupling of SA to H2O2 and glutathione indicates a role for
SA not only in pathogen defence signalling, but also in light
acclimation and in regulating redox homeostasis. The term
redox homeostasis as used here addresses quite severe redox
imbalances. Acclimation to excess excitation energy (EEE)
in Arabidopsis involves local and systemic responses. It is
assumed that damaged chloroplasts initiate the signalling to
the nucleus to suppress expression of photosynthetic genes
(Pogson et al., 2008). An additional light-dependent input
is provided by cryptochrome and phytochrome, which control the expression of diverse nuclear photosynthetic genes
including the small subunit of ribulose-1,5-bisphosphate
carboxylase (Martínez-Hernández et al., 2002; Berry et al.,
2013).
Retrograde signalling in metabolic
adjustment
In contrast to the signals discussed in the previous section,
which are tentatively linked to chloroplast damage, severe
stress, and cell death, another set of signalling molecules
may be considered as immediate process parameters allowing
for feedback control of photosynthetic processes by tuning
involving committed reactions under less stressful conditions
(Dietz et al., 2001) (Figs 2 and 3). This group of signals comprises the altered redox state of intersystem electron transport, redox information from metabolites downstream of
PSI, and signalling pathways linked to changes in metabolite
concentration and sugar accumulation; they are tentatively
defined as ‘primary signals’ (Karpinski et al., 1997, 1999).
Redox-dependent signalling has been known for many
years. The plastoquinone redox state sensitively responds to
environmental cues such as light, CO2, and O2 (Dietz et al.,
1985). Moderate changes in the redox state of the plastoquinone pool in response to light preferentially exciting either
PSI or PSII correlates with alterations in gene expression (Fey
et al., 2005). Transcripts from a set of 2133 genes responded
to the shift from PSI to PSII light with 1121 upregulated and
1012 downregulated genes (Fey et al., 2005). The set of upregulated transcripts included genes for amino acid, nucleotide,
energy, and photosynthetic metabolism (Fey et al., 2005). The
STN7 and STN8 protein kinases sense the reduction state of
the plastoquinone pool and affect short-term acclimation,
while STN7 also participates in long-term acclimation of
photosynthesis (Bonardi et al., 2005; Pesaresi et al., 2009).
Unaltered thiol and glutathione contents and glutathione
reduction states in PSII-light, PSI-light, and under PSIIPSI shift conditions indicate that this type of signalling does
not involve ROS formation (Fey et al., 2005). In addition to
Timeline of light acclimation | 2405
redox stimuli, increasing evidence suggests that ABA represents a link between light excitation pressure, photochemical quenching, and the state of the xanthophyll cycle (Hobe
et al., 2006). Zeaxanthin epoxidase converts zeaxanthin to
violaxanthin. Neoxanthin synthase generates 9′-cis neoxanthin, which is the predominant substrate to 9′-cis epoxycarotenoid dioxygenase (NCED), which produces neoxanthin
(Schwartz et al., 1997). Following export to the cytosol,
neoxanthin is oxidized to ABA in two steps catalysed by xanthoxin oxidase and abscisic aldehyde oxidase (North et al.,
2007). When analysing the expression of responsive genes
after 24 h high light treatment, 81% required photosynthetic
electron transport for their regulation. This group included
the bundle sheath-specific ascorbate peroxidase APX2. 68%
were responsive to ABA (Bechthold et al., 2008). Thus there
was a significant overlap between ABA- and PET-dependent
regulation. Apparently expression of high light-responsive
genes depends on both photosynthetic electron transport and
ABA. In subsequent work, expression of APX2 was linked
to ROS production in the vascular bundles, with ABA as the
signal which spreads from the vascular tissue to the bundle
sheath (Galvez-Valdivieso et al. 2009).
Timing the response in retrograde
signalling
Efficient acclimation to light is achieved by appropriate timing of the response programme (Falkowski and Chen, 2003).
Light-shift experiments allow for time-resolved monitoring
of events that trigger and realize light acclimation. Several
considerations are needed to optimize the experimental
design. Many metabolic and molecular processes in plants
are subject to circadian control (Müller et al., 2014), and
thus harvesting times should be normalized to minimize circadian effects. Light variation is inevitably connected to temperature changes. However, such effects can be minimized
by efficiently blocking infrared light or using light-emitting
diodes. In addition analyses of the high light response after
transfer to the same light intensity using Arabidopsis plants
that had been acclimated to very low or intermediate growth
light excluded differential heating effects when comparing
different light jumps. Using Arabidopsis plants acclimated
to either shade or intermediate light were transferred to the
same high light corresponding to either a 100- or 10-fold light
increase (Oelze et al., 2012) (Fig. 4). The acclimation response
depends on hierarchical execution of events. Fast activation
of preexisting signalling pathways and transcription factors
triggers early expression responses. These early-responsive
transcripts realize second and subsequent waves of expression changes which finally realize acclimation. A simplified
schematic of this hierarchy is shown in Fig. 4B. Detailed
transcriptional profiling and clustering allows researchers to identify candidates (Fig. 4C). The mRNA of the
APETALA 2/ETHYLENE RESPONSE FACTOR (AP2/
ERF) transcription factor RAP2.4a belongs to a network of
extremely fast-responding transcription factors (Vogel et al.,
2014). With significant delay, the amount of RAP2.6 mRNA
Fig. 4. Experimental set up, theoretical response cascade, and transcript
responses in a light-shift experiment. (A) Arabidopsis plants were either
acclimated to low light near light compensation point (8 µmol quanta m–2
s) or continued to be grown in growth chamber light (80 µmol quanta
m–2 s), and then transferred to high light (800 µmol quanta m–2 s), which
corresponds to a 100- or 10-fold light increment. The leaf responses at
various molecular levels are analysed in a time-dependent manner. (B)
Theoretical consideration shows that several levels of response cooperate
in realizing the ultimate acclimation. Here it is suggested that constitutive
transcription factors (TFs) are directly activated by retrograde signals. At
the second level cascading transcription factors are upregulated, and
finally trigger the expression change needed for the acclimation response.
(C) The patterns are reflected by the transcript levels of example genes
such as rapidly responding RAP2.4a, delayed responding RAP2.6, and
final upregulation of sAPX. Activation of the preexisting transcription factor
is only indirectly indicated by the upregulation of RAP2.4a (Vogel et al.,
2014, Alsharafa et al., 2014).
is upregulated. Finally, the transcript of stromal ascorbate
peroxidase (sAPX) accumulates. These examples for distinct kinetics do not describe dependencies, but they are a
good demonstration of the hierarchical activation of light
2406 | Dietz
acclimation responses. It should also be noted that changes
in transcript amounts do not necessarily translate into proportional changes in protein levels (Oelze et al., 2014).
Metabolites as signals acting at all
time scales
The metabolism of photosynthesizing cells changes immediately upon alteration of photosynthetic conditions, in particular light, temperature, or CO2 availability, which depends
on the state of stomatal opening (Dietz and Heber, 1984).
Thus, the metabolic state is an ideal candidate to provide signals for retrograde transfer from the chloroplast to the cytosol and nucleus. Metabolism provides information at time
scales ranging from very fast to slow. Studies using 14CO2labelling conducted in the 1950s, e.g. by Melvin Calvin, James
Bassham, and Andrew Benson, and then in the 1980s with
isolated chloroplasts, non-aqueously prepared subcellular
fractions, and sensitive biochemical metabolite profiling provided detailed information on time-, CO2- and temperaturedependencies of subcellular metabolite pools. Autocatalytic
buildup up of Calvin cycle intermediates upon transfer of
chloroplasts, algae and leaves, respectively, from darkness
to light involves the activation of regulatory enzymes. The
amounts of 3-phosphoglycerate (3-PGA) depend on the carboxylation rate. 3-PGA is converted to ­
dihydroxyacetone
phosphate (DHAP) by ATP-dependent phosphorylation and
NADPH-dependent reduction. Thus DHAP is a high-energy
compound which is exported to the cytosol. The enzymatic
cascade consisting of glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase, and triosephosphate
isomerase allows for synthesis of ATP from ADP and Pi and
NAD(P)H + H+ from NADP+ in the cytosol (Heber, 1974;
Heineke et al., 1991). DHAP as measured in chloroplasts
that had been non-aqueously prepared from darkened leaves
is below the detection limit of enzymatic assays. Upon illumination of darkened leaves, stromal DHAP peaks within
10 s (Dietz and Heber, 1984). Immediate metabolic changes
transmit information on redox state, phosphorylation potential, and carbohydrate status from the chloroplast to the
cytosol. A co-expressed network of AP2/ERF transcription
factors was shown to comprise early-responding transcripts
that could serve as a readout of rapid retrograde signalling.
Its transcriptional regulation was exploited in combination
with genetic mutants defective in specific elements to elucidate retrograde signalling. The triosephosphate/phosphate
translocator, which catalyses the export of DHAP, acted as a
block, interrupting fast retrograde signalling upon low light
to high light transfer (Vogel et al., 2014). The signal which
triggers the transcriptional response of AP2/ERF after
10 min is released after 10 s of high light treatment (Moore
et al., 2014) (cf. Fig. 5). Several transporters link the metabolome of the chloroplast with that of the cytosol in addition
to the triosephosphate phosphate translocator (Weber and
Linka, 2011). The dicarboxylate carrier exchanges malic acid
for oxaloacetate. By coupling this counterport to the activity
of malate dehydrogenase in the stroma and cytosol, reducing
Fig. 5. Dissection of time of no return of high light-triggered transcript
accumulation. Experimental design for the definition of the time period in
high light needed for triggering the upregulation of downstream targets
peaking at t = 10 min. Plants are transferred to high light and harvested or
returned back to low light and harvested at t = 10 min. Direct harvesting
reveals slight upregulation after 5 min and maximal activation after 10 min.
The same transcript level is achieved by 2 min high light followed by 8 min
low light, indicating that the signal is released within 2 min (Vogel et al.,
2014). In fact more detailed analysis shows that the signal is triggered
within a few seconds (Moore et al., 2014).
equivalents can be exported if the reducing power increases
in the chloroplast due to imbalanced NADPH oxidation in
the Calvin cycle and other metabolic pathways (Scheibe and
Dietz, 2012). Interruption of the malate valve in mdh mutants
suppressed the high light-induced accumulation of ERF104
transcript, while other AP2/ERFs of the early-responding
network were unaffected (see Supplementary Figure 3 in
Vogel et al., 2014). Thus triose-phosphate and malate export
feed into distinct signalling pathways during early high light
acclimation.
On a longer time scale of hours, sugars, as the end products
of photosynthesis, play decisive roles in controlling nuclear
gene expression (Ramon et al., 2008). Sugars represent information-rich signalling molecules since they reflect the balance
between carbohydrate supply and consumption in growth
and storage processes. Glucose-dependent signalling depends
on hexokinase1 (HXK1) as a sensor. Sugars interfere with
protein phosphorylation cascades as mediators of sugardependent responses. The protein kinases KIN10 and KIN11
sense energy and are inactivated by glucose. The protein
kinase ‘target of rapamycin’ (TOR) is activated by glucose
(Sheen, 2014). In addition to several cytosolic mechanisms
of sugar sensing, including sensory systems for fructose,
glucose, sucrose, and raffinose, increasing evidence suggests
that sugar levels are also monitored in the plastids (Häusler
et al., 2014). The plastidic hexokinase pHXK participates in
Timeline of light acclimation | 2407
retrograde regulation of nuclear gene expression. A combination of chloramphenicol and 3% glucose effectively suppresses expression of nuclear photosynthetic genes in the wild
type but not in phxk mutants (Zhang, 2010). The rapidity of
response cannot be deduced from these experiments since
glucose and effectors were fed to roots for 48 h. Since glucose
is not a prime product of photosynthesis in chloroplasts, it is
suggested that this sugar is taken up from the cytosol by as
yet unknown transporters (Häusler et al., 2014).
2-C-methyl-D-erythritol 2,4-cyclodiphosphate (MEcPP),
an intermediate of the methylerythritol phosphate pathway,
is another metabolite suggested to function as a retrograde
signal from the chloroplast to the nucleus. It accumulates in
leaves exposed to high light particularly in combination with
heat (Rivasseau et al., 2009). Published reports mostly focus
on later time points of stress treatment between 45 min and
4 h. MEcPP levels need to be measured at early time points
following transfer to high light to assess its possible function
in fast retrograde signalling. MEcPP functions as a retrograde
signal on an intermediate time scale of hours, controlling
nuclear gene expression, such as expression of hydroperoxide
lyase (Xiao et al., 2012). It is apparent from these examples
that metabolite signalling participates decisively in short- and
long-term light acclimation.
Redox and ROS as signals in fast and
intermediate responses
Redox changes of photosynthetic electron transport components occur immediately after altering incident light intensities. The multiphasic kinetics of chlorophyll fluorescence
indicates ultra-rapid changes in the redox state of primary
acceptors of PSII. Thus generation of ROS may occur on even
faster time scales than changes in metabolites. Singlet oxygen
(↑O2) generation is detected by radical trapping and electron
spin resonance quantification within 1 min of the start of
illumination (Ramel et al., 2013). Pre-illumination moderated the ↑O2-induced transcriptional response, indicating
acclimation to singlet oxygen-induced stress. Upregulation
of ↑O2-indicating marker transcripts was maintained for 2
d in a chlorophyll b-deficient mutant (Ramel et al., 2013).
Apparently a persistent role in light acclimation may be
assigned to ↑O2. Interestingly, the signalling role of ↑O2 is
not restricted to illuminated chloroplasts. Transcriptome
signatures and fluorescence of Singlet Oxygen Sensor Green
indicate that ↑O2 derives from various subcellular compartments including mitochondria and can be generated in a
light-independent manner (Mor et al., 2014). Superoxide
and hydrogen peroxide are rapidly generated in chloroplasts
upon illumination and probably transmit information from
chloroplasts to the cytoplasm and nucleus. Isolated chloroplasts release H2O2 immediately (<1 min) upon illumination, as shown by an increase in resorufin fluorescence and
detection of electron paramagnetic resonance signals from
H2O2-derived hydroxyl radicals (Mubarakshina et al., 2010).
Heyno et al. (2014) suggested an intriguing hypothesis of
retrograde-controlled H2O2 accumulation by inhibition of
peroxisomal catalase. Following overreduction of the chloroplast in the light, the export of reducing power via the malate
valve might trigger the thioredoxin-dependent inhibition of
catalase. This in turn would enhance release of an H2O2
signal from the peroxisome. This hypothesis is supported
by a lack of H2O2 accumulation in illuminated protoplasts
obtained from plants with a defective malate valve, while
in wild type protoplasts H2O2 accumulates within 10 min
(Heyno et al., 2014). Light-induced H2O2 also originates
from the apoplast-facing NADPH oxidase of bundle sheath
cells and activates expression of light-induced transcripts
(Fryer et al., 2003; Bechthold et al., 2008). Thus the ROSsignalling network in light acclimation comprises different
ROS, is triggered from distinct subcellular and cellular sites,
activates light responses on variable time scales, and induces
specific response patterns (op den Camp, 2003). Proteomics
approaches have allowed for identification of proteins sensitive to low ROS concentrations, e.g. peroxiredoxins and
cyclophilin Cyp20-3 (Muturamalingam et al., 2013).
In addition to ROS signals, light-induced redox changes
also control light acclimation processes. In fact redox regulation may be considered to occur prior to ROS regulation. The
redox state of intersystem electron transport controls shortterm acclimation such as state transitions within a few minutes and long-term acclimation within hours (Pesaresi et al.,
2009). Backhausen et al. (1994) investigated the hierarchy of
electron distribution from light-driven electron transport to
electron-consuming processes in isolated chloroplasts. The
priority of events as correlated with increasing reduction
potential was: (i) detoxification by reduction of H2O2; (ii)
activation of reductive carbon and nitrogen metabolism; (iii)
activation of the malate valve for export of excess reducing
power; (iv) increased ratio of cyclic to linear electron flow;
and only with lowest priority (v) transfer of electrons to O2
to produce superoxide and hydrogen peroxide (Backhausen
et al., 1994). These responses occur within fractions of minutes. Redox information also integrates information on longer
time scales. Changes in ascorbate and glutathione levels and
redox state are examples of redox signals that coordinate cell
processes on longer time scales. The increase in ascorbate and
glutathione levels upon transfer of plants to high light occurs
within an hour when the plants are transferred from normalgrowth light to high light. The increase is delayed by 3 h if
the plants have previously been acclimated to very low light
intensities (Alsharafa et al., 2014). Redox signals control, e.g.,
the expression of photosynthetic genes and thus light acclimation (Queval and Foyer, 2012).
Hormones as core messengers of light
acclimation
Hormones coordinate environmental acclimation and tailored development. Plant hormones participate in light acclimation and have been identified as retrograde signals. The
role of ABA, SA, and oxylipins is well documented. The
most rapid change in hormone levels upon transfer to high
light was observed for oxylipins. Within 10 min following
2408 | Dietz
the light shift, the chloroplast intermediate of the JA pathway oxophytodienoic acid (OPDA) rises (Alsharafa et al.,
2014) indicating immediate release of α-linolenic acid by
an as yet unidentified light-dependent process and conversion of α-linolenic acid by 13-lipoxygenase, alleneoxide synthase, and alleneoxide cyclase to OPDA (Schaller and Stintzi,
2009). Feeding of OPDA to the moss Physcomitrella patens
altered the abundance of 84 proteins mostly involved in photosynthetic functions (Toshima et al., 2014). OPDA regulates processes independent of further processing to JA, e.g.
biotic defence (Bosch et al., 2014). OPDA binds to the single
stromal cyclophilin Cyp20-3. The OPDA-Cyp20-3 complex
activates the cysteine synthase complex (Park et al., 2013).
The subsequent steps are not yet clear. Finally glutathione
pools increase and the thiol redox environment of the cells
gets more reducing, which in turn triggers gene expression
and fosters defence reactions (Park et al., 2013).
The major route of ABA synthesis starts with 9′-cis neoxanthin in the chloroplast (Milborrow, 2001). Violaxanthin
is a precursor for synthesis of both the non-photochemical
quencher of light-harvesting zeaxanthin and also of ABA.
ABA functions in light acclimation both in retrograde signalling from the chloroplast to the nucleus and in signalling
from the bundle sheath to the mesophyll. ABA levels increase
within 15 min of transfer of Arabidopsis from 150 to 750 µmol
quanta m–2 s, but only if the relative humidity is low (GalvezValdivieso et al., 2009). The authors concluded that ABA
synthesis mediates the high light acclimation of mature leaves
if relative humidity is low. Interestingly, inhibition of NCED
suppresses ABA accumulation and bundle sheath-derived
accumulation of H2O2 (Galvez-Valdivieso et al., 2009) leading to the conclusion of an ABA-dependency of extracellular
H2O2 accumulation in the veins. The increase in ABA is also
observed in transfer experiments where Arabidopsis was subjected to a 10- or 100-fold light increment, but slightly delayed
compared to the report by Galvez-Valdivieso et al. (2009).
The increase was more pronounced in an experiment employing the 10-fold light increment (Alsharafa et al., 2014). It is
also of interest that the amount of ABA-marker transcript
COR47 decreased during the 6 h experiment. This could suggest trapping of ABA in the alkaline chloroplast, meaning
delayed release of ABA-triggered information (Heilmann
et al., 1980). Interestingly, ABA also exerts functions in the
chloroplast as it suppresses expression of plastome-encoded
genes (Yamburenko et al., 2013).
Leaf SA levels are unchanged during low-to-high light
transfer experiments (Alsharafa et al., 2014). Thus rapid
changes in SA may not play a role as retrograde signals
from the chloroplast to the nucleus in the early high light
acclimation response. However, as discussed above, SA levels control light acclimation in the long term as shown in
SA-accumulating Arabidopsis mutants cpr1-1, cpr5-1, cpr61, and dnd1-1 (Mateo et al., 2006). Their dwarf phenotype
is overcome in high light. The authors showed a strong link
between high ROS, glutathione, and SA levels (Mateo et al.,
2006).
Gibberellin and auxin functions are tightly linked to carbohydrate, redox, and energy signalling (Tognetti et al., 2012) and
thus it is not surprising that in the long run changes in light
availability control the developmental programme of the shoot
and root system. External application of the gibberellic acid
GA3 on the leaf surface of broad bean or soybean stimulated
photosynthesis within 1 h. Inhibition of translation abolished
the stimulation of photosynthesis by GA3, while suppression
of transcription through simultaneous treatment with actinomycin D was ineffective. Yuan and Xu (2001) concluded that
GA3 activates photosynthesis by stimulating the translation of
photosynthesis genes. The significance of this GA3 effect in the
natural light environment needs to be assessed in future work
employing specific mutants and natural variation.
C-repeat/dehydration-responsive element binding transcription factors (CBF/DREB1s) participate in the process
of light acclimation particularly at low temperatures. They
are suggested to coordinate phytochrome-dependent, redox,
and hormonal signalling as shown in winter-hardy cereals
(Kurepin et al., 2013).
The above review sections have described available data
on the speed of signal release. Figure 6 attempts to sort 16
signals which have been discussed along a timeline covering
milliseconds to days following a major light intensity shift. It
can be seen that redox- and ROS-related signals tend to react
rather rapidly, while hormones cluster heterogeneously in the
intermediate and long time range.
Translational control in response to light:
long known for plastids but a novel target
of retrograde signalling
Translation is under the control of light-dependent redox signals (Danon and Mayfield, 1994). Singlet oxygen inhibits the
repair cycle of the PSII reaction centre in Synechocystis by
inhibiting translational elongation of D1-protein (Nishiyama
et al., 2004). Within 15 min after transfer of Chlamydomonas
from low growth light to high light, synthesis of the Rubisco
large subunit is suppressed and synthesis of D1 protein
enhanced to facilitate the D1 repair cycle (Shapira et al.,
1997). In Chlamydomonas, translation of light-harvesting
complex proteins of PSII (LHCII) is under the control of a
translational repressor (Wobbe et al., 2009). Although this
particular repressor-dependent mechanism has not been
detected in higher plants, translation is suggested to be under
redox control. Kojima et al. (2009) observed redox-dependent
elongation via thioredoxin-linked redox changes of elongation factor G (elF-G) in Synechocystis. Significant evidence
indicates that eukaryotic translational initiation factors and
elFs are under redox and phosphorylation/dephosphorylation control (Yamazaki et al., 2004; Rouhier et al., 2005; BoexFontvieille et al., 2013). Phosphopreoteome analysis reveals
a correlation between the phosphorylation state of eIF3,
eIF4A, eIF4B, eIF4G, and eIF5 and photosynthetic activity
(Boex-Fontvieille et al., 2013). Phosphorylation of some sites
positively correlates with photosynthetic activity, while others
are negatively correlated. To assess the translational efficiency
following a 10- or 100-fold light intensity increase, changes
in de novo-synthesized proteins were compared with changes
Timeline of light acclimation | 2409
Fig. 6. Tentative timeline of signals involved in light acclimation. Photochemistry changes the state of photosynthetic components within milliseconds
after changes in light intensity. Plastoquinone (PQ) redox state and singlet oxygen are the first signals that are sensed. Metabolic regulation depends on
products of light reactions (ATP, NADPH); dihydroxyacetone phosphate is released from the chloroplast as retrograde signal. Thioredoxin (Trx)-linked
signalling has been proposed. H2O2 and OPDA levels increase within minutes. Concentrations of JA, ABA, and MEcPP change after somewhat less than
an hour, while sugars, SA, and auxin respond late.
in transcript levels of nucleus-encoded chloroplast proteins
(Oelze et al., 2014). In most cases regulation at the transcript
level was larger than regulation at the level of de novo protein
synthesis. O-acetylserine thiol lyase B and heat shock protein
70 are examples of larger increases in de novo protein synthesis than in transcript amounts (Oelze et al., 2014). Apparently
translational control is highly significant in retrograde adjustment of metabolism to changing light intensities.
Translational control is conditionally superior to transcriptional regulation for at least two reasons: faster response time
and potential subcellular heterogeneity (Fig. 7). Preferential
ribosome loading exploits the preexisting RNA population to
synthesize those proteins which are most appropriate for the
new environmental conditions. It has been shown that signals
derived from photosynthesis control the association of ferredoxin mRNA with the polysomal fraction and thus ferredoxin synthesis (Petracek et al., 1997). Many chloroplasts,
mitochondria, and other compartments in each cell emit
retrograde signals which encode information on their specific
metabolic state. Thus, retrograde signalling from organelles
to nuclear gene expression averages retrograde signal intensities from many organelles, as discussed above. It appears to
be a reasonable hypothesis that retrograde control of translation could allow for a response to spatially inhomogeneous
retrograde signals. Thereby protein synthesis could show
local heterogeneity, e.g. if local production of ROS in bundle
sheath cells in connection with cellular antioxidant defence
establishes redox gradients within a cell.
Distinguishing stochastic fluctuations from
long-lasting changes
Dynamic acclimation to the environment must rely on both
rapid response mechanisms and time delay mechanisms. Let
us consider a single light fleck occasionally hitting a shade
leaf. This event should not initiate the transition to sun leaf
characteristics. On the other hand the onset of high light may
indicate the beginning of a long lasting and profound change
in environmental conditions, necessitating immediate action
for maintaining fitness. Thus, on the one hand, there is a need
to immediately and sensitively sense acute changes and subsequently elicit fast responses. On the other hand, time-delay
sensing should integrate the overall parameter intensity and
realize appropriate long-term acclimation. Redox and ROS
are candidates for short-term immediate signalling, while
accumulating sugars may function as integrating signals.
Conquest of new frontiers in network
understanding
The initial concept of retrograde signalling was based on
plastid factors that are needed for full expression of the
(chloro-)plastidic complement of nuclear genes (Hagemann
and Börner, 1978). Later on, central regulators were proposed
to control plastid-to-nucleus communication which include
genome uncoupled 4 (GUN4), ABA insensitive 1 and 4 (ABI1
and ABI4), redox responsive transcription factor (RRTF),
and the executer proteins EX1 and EX2, which mediate a
response to acute toxic singlet oxygen doses (op den Camp
et al., 2003; Baier and Dietz, 2005; Koussevitzky et al., 2007;
Khandelwal et al., 2008; Giraud et al., 2009; Pfannschmidt,
2010). Figure 8 summarizes key processes and events in light
acclimation as recently described (Oelze et al., 2012, 2014;
Alsharafa et al., 2014; Vogel et al., 2014). The basic question
concerns the validity of the concept of retrograde signalling in long-term acclimation (Kleine et al., 2009). The work
addressed in this review shows that activation of short-term
responses in the extraplastidic compartments, in particular
the cytosol and the nucleus, can be linked to specific chloroplast-derived signalling entities such as metabolites, ROS,
2410 | Dietz
Fig. 7. Theoretical comparison of retrograde control of translation relative to nuclear transcription. The figure shows a photosynthesizing cell with many
organelles and a single nucleus. Retrograde control of nuclear gene expression depends on multiple signals that are released from many organelles
and finally taken into account in an integrated manner. It might be a possibility that organelles near the nucleus exert a stronger influence than distant
organelles. In a converse manner, retrograde control of translation is likely to be under the immediate control of vicinal organelles. The cytoplasm shows
a gradient of red to green, which symbolizes the uneven distribution of signals (e.g. redox, ROS) which may be released on the right-hand side by higher
incident light and is buffered by mechanisms of redox homeostasis. According to this scenario, ribosomes in the red area would translate different
mRNAs to ribosomes in the green area.
Fig. 8. Timeline of acclimation response of leaves after transfer to high light. The transcriptomes of low and normal light-acclimated plants are highly
similar after 6 h of high light treatment (Oelze et al., 2014). Kinetic analysis of molecular and biochemical features dissects the response behaviour of
participating mechanisms: ultrafast release of metabolites, transient accumulation of ROS, the point of no return, oxidation of H2O2-sensitive targets,
preferential ribosome loading, increase in OPDA concentration, maximal expression of early-responding transcription factors, activation of redox-sensitive
transcription factors, reorganization of translated proteome, and finally adjustment of transcriptome. While evidence exists for each step, the precise
order and dependencies still await further clarification (Shaikhali et al., 2012; Muturamalingam et al., 2013; Alsharafa et al., 2014; Oelze et al., 2014;
Vogel et al. 2014).
Timeline of light acclimation | 2411
redox changes of particular biochemical elements, and cell
energization. In long-term acclimation, these mechanisms
interfere and are part of general acclimation programmes.
Improved photosynthesis inevitably affects the entire plant.
Acclimation to progressive water deficit may be taken as an
example, and involves ABA-dependent and -independent
pathways. These pathways deploy redox and calcium signalling. Glutathione peroxidase 3 feeds information into the
ABA-signalling pathway by oxidizing ABI1/2 in the presence
of H2O2 (Miao et al., 2006). The CALCIUM DEPENDENT
PROTEIN KINASE 21 (CPK21) is controlled by thioredoxin h1 (Ueoka-Nakanishi et al., 2013). CPK21 regulates
ion channels which control osmotic relations. Thus redox and
ABA signalling are tightly linked and both depend on chloroplast activities. This type of signal processing should not
be termed retrograde signalling in its proper sense. It rather
reflects the central position of chloroplasts in plant metabolism and thus the unsurprising fact that chloroplast metabolism is central in controlling plant cell responses on all time
scales.
Experimental designs with excess excitation energy relative
to growth light offer important approaches for elucidating
signalling pathways, networks, and physiological mechanisms
needed for plants to acclimate to high photon flux densities.
The complexity and redundancy of the activation mechanism
explains why plants (usually) cope efficiently with full sunlight following acclimation.
Berry JO, Yerramsetty P, Zielinski AM, Mure CM. 2013.
Photosynthetic gene expression in higher plants. Photosynthesis Research
17, 91–120.
Acknowledgements
Dietz K-J, Heber U. 1984. Rate-limiting factors in leaf photosynthesis:
Carbon fluxes in the Calvin Cycle. Biochimica et Biophysica Acta 767,
432–443.
The work of the author cited in this review originates from cooperation
within the Research Focus Retrograde Signalling and was funded by the
DFG (DI346, FOR804, FOR 1710).
References
Alsharafa A, Vogel MO, Oelze ML, Moore M, Stingl N, König K,
Friedman H, Mueller MJ, Dietz KJ. 2014. Kinetics of retrograde
signalling initiation in the high light response of Arabidopsis thaliana.
Philosophical Transactions of the Royal Society of London 369,
20130424.
Anderson JM, Chow WS, Park YI. 1995. The grand design of
photosynthesis: Acclimation of the photosynthetic apparatus to
environmental cues. Photosynthesis Research 46, 129–139.
Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen
V, Saleem A, Battchikova N, Rintamäki E. 2005. Dynamics of
photosystem II: a proteomic approach to thylakoid protein complexes.
Journal of Experimental Botany 56, 347–356.
Backhausen JE, Kitzmann C, Scheibe R. 1994. Competition between
electron acceptors in photosynthesis: Regulation of the malate valve
during CO2 fixation and nitrite reduction. Photosynthesis Research 42,
75–86.
Baier M, Dietz KJ. 2005. Chloroplasts as source and target of
cellular redox regulation: a discussion on chloroplast redox signals in
the context of plant physiology. Journal of Experimental Botany 56,
1449–1462.
Baier M, Stroher E, Dietz KJ. 2005. The acceptor availability at
photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin
A in Arabidopsis thaliana. Plant Cell Physiology 45, 997–1006.
Bechtold U, Richard O, Zamboni A, Gapper C, Geisler M, Pogson
B, Karpinski S, Mullineaux PM. 2008. Impact of chloroplastic- and
extracellular-sourced ROS on high light-responsive gene expression in
Arabidopsis. Journal of Experimental Botany 59, 121–133.
Boardman NK. 1977. Comparative photosynthesis of sun and shade
plants. Annual Review of Plant Biology 28, 355–377.
Boex-Fontvieille E, Daventure M, Jossier M, Zivy M, Hodges M,
Tcherkez G. 2013. Photosynthetic control of Arabidopsis leaf cytoplasmic
translation initiation by protein phosphorylation. PLoS One 8, e70692.
Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt
T, Jahns P, Leister D. 2005. Photosystem II core phosphorylation and
photosynthetic acclimation require two different protein kinases. Nature
437, 1179–1182.
Bosch M, Wright LP, Gershenzon J, Wasternack C, Hause
B, Schaller A, Stintzi A. 2014. Jasmonic acid and its precursor
12-oxophytodienoic acid control different aspects of constitutive and
induced herbivore defenses in tomato. Plant Physiology 166, 396–410.
Bräutigam K, Dietzel L, Kleine T, et al. 2009. Dynamic plastid redox
signals integrate gene expression and metabolism to induce distinct
metabolic states in photosynthetic acclimation in Arabidopsis. The Plant
Cell 21, 2715–2732.
Brzezowski P, Schlicke H, Richter A, Dent RM, Niyogi KK, Grimm B.
2014. The GUN4 protein plays a regulatory role in tetrapyrrole biosynthesis
and chloroplast-to-nucleus signalling in Chlamydomonas reinhardtii. The
Plant Journal 79, 285–298.
Buchanan BB, Balmer Y. 2005. Redox regulation: a broadening horizon.
Annual Reviews of Plant Biology 56, 187–220.
Danon A, Mayfield SP. 1994. Light-regulated translation of chloroplast
messenger RNAs through redox potential. Science 266, 1717–1719.
del Río LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB. 2003.
Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB
Life 55, 71–81.
Demmig B, Winter K, Krüger A, Czygan FC. 1987. Photoinhibition and
zeaxanthin formation in intact leaves: a possible role of the xanthophyll
cycle in the dissipation of excess light energy. Plant Physiology 84,
218–224.
Dietz K-J, Link G, Pistorius EK, Scheibe R. 2001. Redox regulation in
oxigenic photosynthesis. Progress in Botany 63, 207–245.
Dietz KJ, Schreiber U, Heber U. 1985. The relationship between the
redox state of QA and photosynthesis in leaves at various carbon-dioxide,
oxygen and light regimes. Planta. 166, 219–226.
Escoubas JM, Lomas M, LaRoche J, Falkowski PG. 1995. Light
intensity regulation of cab gene transcription is signaled by the redox
state of the plastoquinone pool. Proceedings of the National Academy of
Sciences, USA 92, 10237–10241.
Falkowski PG, Chen YB. 2003. Photoacclimation of light harvesting
systems in eukaryotic algae. In: Green BR, Parson WW, eds. Advances in
Photosynthesis and Respiration 13, 423–447.
Fey V, Wagner R, Brautigam K, Wirtz M, Hell R, Dietzmann A,
Leister D, Oelmuller R, Pfannschmidt T. 2005. Retrograde plastid
redox signals in the expression of nuclear genes for chloroplast proteins of
Arabidopsis thaliana. The Journal of Biological Chemistry 280, 5318–5328.
Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker
NR. 2003. Control of ascorbate peroxidase 2 expression by hydrogen
peroxide and leaf water status during excess light stress reveals a
functional organisation of Arabidopsis leaves. The Plant Journal 33,
691–705.
Galvez-Valdivieso G, Fryer MJ, Lawson T, et al. 2009. The high light
response in Arabidopsis involves ABA signaling between vascular and
bundle sheath cells. The Plant Cell 21, 2143–2162.
Giraud E, Van Aken O, Ho LH, Whelan J. 2009. The transcription factor
ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE
OXIDASE1a. Plant Physiology 150, 1286–1296.
Glazebrook J. 2005. Contrasting mechanisms of defense against
biotrophic and necrotrophic pathogens. Annual Review of Phytopathology
43, 205–227.
Hagemann R, Börner T. 1978. Plastid ribosome-deficient mutants of
higher plants as a tool in studying chloroplast biogenesis. In: Akoyunoglou
2412 | Dietz
G, Argyroudi-Akoyunoglou JH, eds. Chloroplast development. Amsterdam:
Elsevier, pp. 709–720.
of a minimal RBCS light-responsive unit activated by phytochrome,
cryptochrome, and plastid signals. Plant Physiology 128, 1223–1233.
Häusler RE, Heinrichs L, Schmitz J, Flügge UI. 2014. How sugars
might coordinate chloroplast and nuclear gene expression during
acclimation to high light intensities. Molecular Plant 7, 1121–1137.
Heber U. 1974. Metabolite exchange between chloroplasts and
cytoplasm. Annual Review of Plant Physiology 25, 393–421.
Heilmann B, Hartung W, Gimmler H. 1980. The distribution of
abscisic acid between chloroplasts and cytoplasm of leaf cells and the
permeability of the chloroplast envelope for abscisic acid. Zeitschrift für
Pflanzenphysiologie 97, 67–78.
Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge UI,
Heldt HW. 1991. Redox transfer across the inner chloroplast envelope
membrane. Plant Physiology 95, 1131–1137.
Heyno E, Innocenti G, Lemaire SD, Issakidis-Bourguet E, KriegerLiszkay A. 2014. Putative role of the malate valve enzyme NADPmalate dehydrogenase in H2O2 signalling in Arabidopsis. Philosophical
Transactions of the Royal Society of London 369, 20130228.
Hobe S, Trostmann I, Raunser S, Paulsen H. 2006. Assembly of the
major light-harvesting chlorophyll-a/b complex: Thermodynamics and
kinetics of neoxanthin binding. The Journal of Biological Chemistry 281,
25156–25166.
Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Oquist
G, Hurry V, Hüner NP. 2012. Implications of alternative electron sinks in
increased resistance of PSII and PSI photochemistry to high light stress
in cold-acclimated Arabidopsis thaliana. Photosynthesis Research 113,
191–206.
Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM.
1997. Photosynthetic electron transport regulates the expression of
cytosolic ascorbate peroxidase genes in Arabidopsis during excess light
stress. The Plant Cell 9, 627–640.
Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G,
Mullineaux P. 1999. Systemic signaling and acclimation in response to
excess excitation energy in Arabidopsis. Science 284, 654–657.
Khandelwal A, Elvitigala T, Ghosh B, Quatrano RS. 2008.
Arabidopsis transcriptome reveals control circuits regulating redox
homeostasis and the role of an AP2 transcription factor. Plant Physiology
148, 2050–2058.
Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok
M, Blajecka K, Herrfurth C, Feussner I, Apel K. 2012. Chloroplasts
of Arabidopsis are the source and a primary target of a plant-specific
programmed cell death signaling pathway. The Plant Cell 24, 3026–3039.
Kleine T, Voigt C, Leister D. 2009. Plastid signaling to the nucleus:
messengers still lost in the mists? Trends in Genetics 25, 185–192.
Kojima K, Motohashi K, Morota T, Oshita M, Hisabori T, Hayashi
H, Nishiyama Y. 2009. Regulation of translation by the redox state of
elongation factor G in the cyanobacterium Synechocystis sp. PCC 6803.
The Journal of Biological Chemistry 284, 18685–18691.
König J, Muthuramalingam M, Dietz KJ. 2012. Mechanisms and
dynamics in the thiol/disulfide redox regulatory network: transmitters,
sensors and targets. Current Opinion in Plant Biology 15, 261–268.
Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins
G, Surpin M, Lim J, Mittler R, Chory J. 2007. Multiple signals from
damaged chloroplasts converge on a common pathway to regulate
nuclear gene expression. Science 316, 715–719.
Kurepin LV, Keshav P, Dahal KP, Savitch LV, Singh J, Bode R,
Ivanov AG, Hurry V, Hüner NPA. 2013. Role of CBFs as integrators of
chloroplast redox, phytochrome and plant hormone signaling during cold
acclimation. International Journal of Molecular Science 14, 12729–12763.
Leister D, Romani I, Mittermayr L, Paieri F, Fenino E, Kleine T.
2014. Identification of target genes and transcription factors implicated in
translation-dependent retrograde signaling in Arabidopsis. Molecular Plant
7, 1228–1247.
Lepistö A, Toivola J, Nikkanen L, Rintamäki E. 2012. Retrograde
signaling from functionally heterogeneous plastids. Frontiers in Plant
Science. 3, 286.
Malkin S, Fork DC. 1981. Photosynthetic units of sun and shade plants.
Plant Physiology 67, 580–583.
Martínez-Hernández A, López-Ochoa L, Argüello-Astorga G,
Herrera-Estrella L. 2002. Functional properties and regulatory complexity
Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM,
Karpinski S. 2006. Controlled levels of salicylic acid are required for
optimal photosynthesis and redox homeostasis. Journal of Experimental
Botany 57, 1795–1807.
McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR,
Hüner NP. 2011. Flexibility in photosynthetic electron transport: the
physiological role of plastoquinol terminal oxidase (PTOX). Biochimica et
Biophysica Acta 1807, 954–967.
Meng PH, Raynaud C, Tcherkez G, et al. 2009. Crosstalks between
myo-inositol metabolism, programmed cell death and basal immunity in
Arabidopsis. PLoS One 4, e7364.
Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp
R, Apel K. 2001. FLU: a negative regulator of chlorophyll biosynthesis in
Arabidopsis thaliana. Proceedings of the National Academy of Science,
USA 98, 12826–12831.
Meskauskiene R, Würsch M, Laloi C, Vidi PA, Coll NS, Kessler F,
Baruah A, Kim C, Apel K. 2009. A mutation in the Arabidopsis mTERFrelated plastid protein SOLDAT10 activates retrograde signaling and
suppresses 1O2-induced cell death. The Plant Journal 60, 399–410.
Miao Y, Lv D, Wang P, Wang X-C, Chen J, Miao C, and Song
C-P. 2006. An Arabidopsis glutathione peroxidase functions as both a
redox transducer and a scavenger in abscisic acid and drought stress
responses. The Plant Cell 18, 2749–2766.
Michelet L, Zaffagnini M, Morisse S, et al. 2013. Redox regulation of
the Calvin-Benson cycle: something old, something new. Frontiers in Plant
Science 4, 470.
Milborrow BV. 2001. The pathway of biosynthesis of abscisic acid
in vascular plants, a review of the present state of knowledge of ABA
biosynthesis. Journal of Experimental Botany 52, 1145–1164.
Moore M, Vogel MO, Dietz KJ. 2014. The acclimation response to high
light is initiated within seconds as indicated by upregulation of AP2/ERF
transcription factor network in Arabidopsis thaliana. Plant Signaling and
Behavior doi: 10.4161/15592324.2014.976479
Mor A, Koh E, Weiner L, Rosenwasser S, Sibony-Benyamini H,
Fluhr R. 2014. Singlet oxygen signatures are detected independent of
light or chloroplasts in response to multiple stresses. Plant Physiology 165,
249–261.
Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR,
Krieger-Liszkay A. 2010. Production and diffusion of chloroplastic
H2O2 and its implication to signalling. Journal of Experimental Botany 61,
3577–3587.
Mühlenbock P, Szechynska-Hebda M, Plaszczyca M, Baudo M,
Mateo A, Mullineaux PM, Parker JE, Karpinska B, Karpinski S.
2008. Chloroplast signaling and LESION SIMULATING DISEASE1 regulate
crosstalk between light acclimation and immunity in Arabidopsis. The Plant
Cell 20, 2339–2356.
Müller LM, von Korff M, Davis SJ. 2014. Connections between
circadian clocks and carbon metabolism reveal species-specific effects on
growth control. Journal of Experimental Botany 65, 2915–2923.
Müller MJ, Berger S. 2009. Reactive electrophilic oxylipins: pattern
recognition and signalling. Phytochemistry 70, 1511–1521
Muthuramalingam M, Matros A, Scheibe R, Mock HP, Dietz KJ.
2013. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro
and in vivo. Frontiers in Plant Science 4, 54.
Nikkanen L, Rintamäki E. 2014. Thioredoxin-dependent regulatory
networks in chloroplasts under fluctuating light conditions.
Philosophical Transactions of the Royal Society of London 369,
20130224.
Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N.
2004. Singlet oxygen inhibits the repair of photosystem II by suppressing
the translation elongation of the D1 protein in Synechocystis sp. PCC
6803. Biochemistry 43, 11321–11330.
North HM, De Almeida A, Boutin JP, Frey A, To A, Botran L, Sotta
B, Marion-Poll A. 2007. The Arabidopsis ABA-deficient mutant aba4
demonstrates that the major route for stress-induced ABA accumulation is
via neoxanthin isomers. The Plant Journal 50, 810–824.
Oelze ML, Muthuramalingam M, Vogel MO, Dietz KJ. 2014. The
link between transcript regulation and de novo protein synthesis in the
Timeline of light acclimation | 2413
retrograde high light acclimation response of Arabidopsis thaliana. BMC
Genomics 15, 320.
Oelze ML, Vogel MO, Alsharafa K, Kahmann U, Viehhauser A,
Maurino VG, Dietz KJ. 2012. Efficient acclimation of the chloroplast
antioxidant defence of Arabidopsis thaliana leaves in response to a 10or 100-fold light increment and the possible involvement of retrograde
signals. Journal of Experimental Botany 63, 1297–1313.
op den Camp RGL, Przybyla D, Ochsenbein C, et al. 2003. Rapid
induction of distinct stress responses after the release of singlet oxygen in
Arabidopsis. The Plant Cell 15, 2320–2332.
Öquist G, Anderson JM, McCaffery S, Chow WS. 1992. Mechanistic
differences in photoinhibition of sun and shade plants. Planta 188,
422–431.
Papenbrock J, Mishra S, Mock HP, Kruse E, Schmidt EK,
Petersmann A, Braun HP, Grimm B. 2001. Impaired expression of the
plastidic ferrochelatase by antisense RNA synthesis leads to a necrotic
phenotype of transformed tobacco plants. The Plant Journal 28, 41–50.
Park SW, Li W, Viehhauser A, et al. 2013. Cyclophilin 20-3 relays a
12-oxo-phytodienoic acid signal during stress responsive regulation of
cellular redox homeostasis. Proceedings of the National Academy of
Science, USA 110, 9559–9564.
Pesaresi P, Hertle A, Pribil M, et al. 2009. Arabidopsis STN7 kinase
provides a link between short- and long-term photosynthetic acclimation.
The Plant Cell 21, 2402–2423.
Petracek ME, Dickey LF, Huber SC, Thompson WF. 1997. Lightregulated changes in abundance and polyribosome association of
ferredoxin mRNA are dependent on photosynthesis. The Plant Cell 9,
2291–2300.
Pfannschmidt T. 2003. Chloroplast redox signals: how photosynthesis
controls its own genes. Trends in Plant Science 8, 33–41.
Pfannschmidt T. 2010. Plastidial retrograde signalling--a true “plastid
factor” or just metabolite signatures? Trends in Plant Science 15, 427–435.
Pogson BJ, Woo NS, Förster B, Small ID. 2008. Plastid signalling to
the nucleus and beyond. Trends in Plant Science 13, 602–609.
Pruzinská A, Tanner G, Anders I, Roca M, Hörtensteiner S. 2003.
Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type ironsulfur protein, encoded by the accelerated cell death 1 gene. Proceedings
of the National Academy of Sciences, USA 100, 15259–15264.
Puthiyaveetil S, Ibrahim IM, Allen JF. 2012. Oxidation-reduction
signalling components in regulatory pathways of state transitions and
photosystem stoichiometry adjustment in chloroplasts. Plant, Cell and
Environment 35, 347–359.
Queval G, Foyer CH. 2012. Redox regulation of photosynthetic gene
expression. Philosophical Transactions of the Royal Society of London
367, 3475–3485.
Ramel F, Ksas B, Akkari E, Mialoundama AS, Monnet F, KriegerLiszkay A, Ravanat JL, Mueller MJ, Bouvier F, Havaux M. 2013.
Light-induced acclimation of the Arabidopsis chlorina1 mutant to singlet
oxygen. The Plant Cell 25, 1445–1462.
Ramon M, Rolland F, Sheen J. 2008. Sugar sensing and signaling. The
Arabidopsis Book 6, e0117.
Rivasseau C, Seemann M, Boisson AM, Streb P, Gout E, Douce R,
Rohmer M, Bligny R. 2009. Accumulation of 2-C-methyl-D-erythritol
2,4-cyclodiphosphate in illuminated plant leaves at supraoptimal
temperatures reveals a bottleneck of the prokaryotic methylerythritol
4-phosphate pathway of isoprenoid biosynthesis. Plant, Cell and
Environment 32, 82–92.
Rouhier N, Villarejo A, Srivastava M, et al. 2005. Identification of plant
glutaredoxin targets. Antioxidants and Redox Signaling 7, 919–929.
Ruban AV, Berera R, Ilioaia C, van Stokkum IH, Kennis JT, Pascal
AA, van Amerongen H, Robert B, Horton P, van Grondelle R. 2007.
Identification of a mechanism of photoprotective energy dissipation in
higher plants. Nature 450, 575–578.
Sane PV, Ivanov AG. Öquist G, Hüner NPA. 2012.
Thermoluminescence. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD,
eds. Photosynthesis: plastid biology, energy conversion and carbon
assimilation. Advances in Photosynthesis and Respiration, Vol 34.
Dordrecht: Springer, pp. 445–474.
Schaller A, Stintzi A. 2009. Enzymes in jasmonate biosynthesis structure, function, regulation. Phytochemistry 70, 1532–1538.
Scheibe R, Dietz KJ. 2012. Reduction-oxidation network for flexible
adjustment of cellular metabolism in photoautotrophic cells. Plant, Cell and
Environment 35, 202–216.
Schlicke H, Hartwig AS, Firtzlaff V, Richter AS, Glässer C, Maier K,
Finkemeier I, Grimm B. 2014. Induced deactivation of genes encoding
chlorophyll biosynthesis enzymes disentangles tetrapyrrole-mediated
retrograde signaling. Molecular Plant 7, 1211–1227.
Schwarzländer M, Finkemeier I. 2013. Mitochondrial energy and redox
signaling in plants. Antioxidants and Redox Signaling 18, 2122–2144.
Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR. 1997.
Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276,
1872–1874.
Shapira M, Lers A, Heifetz PB, Irihimovitz V, Osmond CB, Gillham
NW, Boynton JE. 1997. Differential regulation of chloroplast gene
expression in Chlamydomonas reinhardtii during photoacclimation: light
stress transiently suppresses synthesis of the Rubisco LSU protein while
enhancing synthesis of the PS II D1 protein. Plant Molecular Biology 33,
1001–1011.
Shaikhali J, Norén L, de Dios Barajas-López J, Srivastava V, König
J, Sauer UH, Wingsle G, Dietz KJ, Strand Å. 2012. Redox-mediated
mechanisms regulate DNA binding activity of the G-group of basic region
leucine zipper. bZIP. transcription factors in Arabidopsis. The Journal of
Biological Chemistry 287, 27510–27525.
Shikanai T. 2014. Central role of cyclic electron transport around
photosystem I in the regulation of photosynthesis. Current Opinion in
Biotechnology 26, 25–30.
Sheen, J. 2014. Master regulators in plant glucose signaling networks.
Journal of Plant Biology 57, 67–79.
Spetea C, Rintamäki E, Schoefs B. 2014. Changing the light
environment: chloroplast signalling and response mechanisms.
Philosophical Transactions of the Royal Society of London 369, 20130220.
Tognetti VB, Mühlenbock P, and Van Breusegem F. 2012. Stress
homeostasis - the redox and auxin perspective. Plant, Cell and
Environment 35, 321–333.
Toshima E, Nanjo Y, Komatsu S, Abe T, Matsuura H, Takahashi
K. 2014. Proteomic analysis of Physcomitrella patens treated with
12-oxo-phytodienoic acid, an important oxylipin in plants. Bioscience
Biotechnology Biochemistry 78, 946–953.
Triantaphylidès C, Havaux M. 2009. Singlet oxygen in plants:
production, detoxification and signaling. Trends in Plant Science 14,
219–228.
Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 2009.
Network properties of robust immunity in plants. PLoS Genetics 5,
e1000772.
Ueoka-Nakanishi H, Sazuka T, Nakanishi Y, Maeshima M,
Mori H, and Hisabori T. 2013. Thioredoxin h regulates calcium
dependent protein kinases in plasma membranes. FEBS Journal 280,
3220–3231.
Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J,
Dietz KJ. 2014. Fast retrograde signaling in response to high light
involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6,
and AP2/ERF transcription factors in Arabidopsis. The Plant Cell 26,
1151–1165.
Weber AP, Linka N. 2011. Connecting the plastid: transporters of
the plastid envelope and their role in linking plastidial with cytosolic
metabolism. Annual Reviews f Plant Biology 62, 53–77.
Weis E, Berry JA. 1987. Quantum efficiency of photosystem II in relation
to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochimica
et Biophysica Acta 894, 198–208
Wobbe L, Blifernez O, Schwarz C, Mussgnug JH, Nickelsen J,
Kruse O. 2009. Cysteine modification of a specific repressor protein
controls the translational status of nucleus-encoded LHCII mRNAs in
Chlamydomonas. Proceedings of the National Academy of Sciences, USA
106, 13290–13295.
Yamazaki D, Motohashi K, Kasama T, Hara Y, Hisabori T. 2004.
Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant
Cell Physiology 45, 18–27.
Yamburenko MV, Zubo YO, Vanková R, Kusnetsov VV, Kulaeva ON,
Börner T. 2013. Abscisic acid represses the transcription of chloroplast
genes. Journal of Experimental Botany 64, 4491–4502.
2414 | Dietz
Yuan L, Xu DQ. 2001. Stimulation effect of gibberellic acid short-term
treatment on leaf photosynthesis related to the increase in Rubisco content
in broad bean and soybean. Photosynthesis Research 68, 39–47.
Xiao Y, Savchenko T, Baidoo EE, Chehab WE, Hayden DM,
Tolshtikov V, Corwin JA, Kliebenstein DJ, Keasling JD, Dehesh K.
2012. Retrograde signaling by the plastidial metabolite MEcPP regulates
expression of nuclear stress-response genes. Cell 149, 1525–1535.
Zhang ZW, Yuan S, Xu F, Yang H, Zhang NH, Cheng J, Lin HH. 2010.
The plastid hexokinase pHXK: a node of convergence for sugar and
plastid signals in Arabidopsis. FEBS Letters 584, 3573–3579.