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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. For permissions, please email: [email protected] 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. 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