Journal of Experimental Botany, Vol. 56, No. 416, pp. 1449–1462, June 2005 doi:10.1093/jxb/eri161 Advance Access publication 29 April, 2005

FOCUS PAPER Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology

Margarete Baier* and Karl-Josef Dietz Biochemistry and Physiology of Plants, University of Bielefeld, D-33501 Bielefeld, Germany

Received 28 January 2005; Accepted 15 March 2005

Abstract Key words: Abscisic acid, antioxidants, chloroplast, gene expression, oxolipin, peroxiredoxin, photosynthesis, redox During the evolution of plants, chloroplasts have lost regulation, signalling, stress. the exclusive genetic control over redox regulation and antioxidant gene expression. Together with many other genes, all genes encoding antioxidant enzymes and enzymes involved in the biosynthesis of low molecular Introduction weight antioxidants were transferred to the nucleus. On the other hand, photosynthesis bears a high risk for In plants, photosynthesis generates redox intermediates photo-oxidative damage. Concomitantly, an intricate with extraordinarily negative redox potentials. Light-driven network for mutual regulation by anthero- and retro- electron transport transfers electrons from the acceptor site grade signals has emerged to co-ordinate the activities of photosystem I (Em < ÿ900 mV) to various acceptors of the different genetic and metabolic compartments. A including oxygen (Em = 815 mV; Blankenship, 2002). The major focus of recent research in chloroplast regula- redox intermediates cover an exceptionally wide range of tion addressed the mechanisms of redox sensing and mid-point redox potentials (Dietz, 2003) with a significant signal transmission, the identification of regulatory risk for electron transfer to oxygen and other appropriate targets, and the understanding of adaptation mech- targets. Among the best known examples for chloroplast anisms. In addition to redox signals communicated redox chemistry is the direct electron transfer from reduced through signalling cascades also used in pathogen ferredoxin to O2 in the so-called Mehler reaction (Mehler, and wounding responses, specific chloroplast signals 1951). The superoxide radicals formed can be quickly control nuclear gene expression. Signalling pathways converted into H2O2 and highly reactive hydroxyl radicals c are triggered by the redox state of the plastoquinone (HO ) (Elstner, 1990). Together with reactive oxygen pool, the thioredoxin system, and the acceptor avail- species (ROS) generated by other sources, they are a con- ability at photosystem I, in addition to control by tinuous threat to cellular constituents for uncontrolled oxolipins, tetrapyrroles, carbohydrates, and abscisic oxidation. acid. The signalling function is discussed in the con- In the context of (i) the physiologically bivalent oxygen text of regulatory circuitries that control the expression chemistry, (ii) the demand for reductive power, and (iii) the of antioxidant enzymes and redox modulators, demon- peril of excess photosynthetic electron pressure, chloro- strating the principal role of chloroplasts as the source plasts are prone to oxidative damage like no other organelle and target of redox regulation. (Foyer et al., 1997). Consequently, photosynthetic organ- isms have evolved defence mechanisms to control the redox poise of the electron transport chain and the redox envir- onment of the stroma. They range from the suppression of

* To whom correspondence should be addressed. Fax: +49 (0)521 106 6039. E-mail: [email protected] Abbreviations: 2CPA, 2-Cys peroxiredoxin A; ABA, abscisic acid; DBMIB, 3-methyl-6-isopropyl-p-benzoquinone; DCMU, 3-(39,49-dichlorophenyl-)1,1- dimethyl urea; DOX, fatty acid dioxygenase; Em, mid-point potential; LOX, lipoxygenase; MAPK(K)(K), mitogen activated protein kinase (kinase) (kinase); NDH, NAD(P)H dehydrogenase; PET, photosynthetic electron transport; PQ, plastoquinone; Prx, peroxiredoxin; ROS, reactive oxygen species; Rubisco, ribulose-1,5-bisphosphate carboxylase oxygenase.

ª The Author [2005]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: [email protected] 1450 Baier and Dietz ROS generation and avoidance of uncontrolled oxidation of essential biomolecules by accumulating high concentra- tions of low-molecular weight antioxidants to repair mech- anisms by reduction and de novo synthesis of damaged molecules. In the illuminated chloroplast, the reduction energy for the regeneration of oxidized metabolites is mainly taken from the photosynthetic electron transport (PET). Depending on the photo-oxidative strain, up to almost 100% of the photosynthetically transported elec- trons can be diverted into the antioxidant defence system (Asada, 2000). In the dark, when the strong reductive power of photosynthesis is missing, the redox environment of chloroplasts probably adjusts to redox potentials similar to those measured in the cytoplasm of heterotrophic cells (i.e. below ÿ300 mV to approximately ÿ240 mV; Dietz, 2003). Under these conditions, chloroplasts stabilize their redox poise by metabolization of starch and import of Fig. 1. The cytosolic antioxidant system shields the nucleus from chloro- plast ROS signals. Photosynthetic ROS signals and redox imbalances are reduction energy. buffered by cytosolic antioxidants. Whether they reach the nucleus Studies with various transgenic plant lines and mutants depends on the rates of ROS-formation and the strength of the cytosolic demonstrated the importance of a high antioxidant cap- antioxidant system. In contrast, a non-redox active second messenger can pass the cytosol without loss of function. acity as realized by low-molecular weight antioxidants (Pastori et al., 2003; Ball et al., 2004) and antioxidant enzymes (Willekens et al., 1997; Baier et al., 2000; may have additional functions, for example, as a metabolic Davletova et al., 2005). The antioxidant defence system re- intermediate. sponds to redox imbalances. The pool size of low molecu- lar weight antioxidants and the expression of chloroplast antioxidant enzymes increases if the photo-oxidative strain Redox coupling on the system is high (Foyer et al., 1997). Interestingly, oxidizing conditions correlate with a high reduction state, All redox active compounds together define the cellular since, as outlined above, excess electrons are transferred redox poise of a cell (Schafer and Buettner, 2001). In to O2 that, in turn, abstract electrons from organic targets. addition to the redox energetics defined by the mid-point This apparent contradiction (‘high reducing activity potentials and the concentrations of the various antioxi- results in oxidizing conditions’) will be important for dants, the redox state of a particular compound is under the understanding redox regulation, as for example in the control of kinetic constraints defining the reaction constants. peroxiredoxin function, in the context of photosynthesis Enzymes lower the kinetic barriers and couple redox pairs. (see below). However, all chloroplast antioxidant enzymes Recycling of oxidized intermediates, as well as regeneration and all enzymes involved in the biosynthesis of low- of the reductants, affect the redox state of specific redox molecular-weight antioxidants are nuclear encoded. The pairs (Dietz, 2003). Different drainage rates of electrons spatial separation of expression and function demands for from antioxidants and weak enzymatic linkages can un- signal transduction over the chloroplast envelope. Devia- couple the redox states of individual components of the tions from regular redox homeostasis can be sensed in the antioxidant network, as has been observed for ascorbate and chloroplast and transmitted to the nucleus by retrograde glutathione. While specific oxidation of the glutathione pool signalling cascades. Alternatively, redox imbalances in the took place in catalase-deficient barley (Willekens et al., chloroplast could be transmitted into the cytoplasm by 1997), reduced 2-Cys peroxiredoxin levels led preferen- metabolic coupling (Fig. 1). The sensor then resides in tially to the oxidation of the ascorbate pool in Arabidopsis the cytoplasm. Transmission of redox signals suffers thaliana (Baier et al., 2000). The favoured oxidation of from the drawback that cytoplasmic redox homeostasis glutathione in the catalase-lines is proposed to be caused by and antioxidant defence will strongly damp the spreading higher cytosolic dehydroascorbate reductase activity rather signal. than glutathione reductase activity, while the redox shift in Another terminology to be clarified is the distinction of the ascorbate pool in the peroxiredoxin antisense plants signalling and regulation. Both terms are used with a broad might be caused by insufficient dehydroascorbate reductase meaning here. Regulation describes any adjustment of activity in the chloroplasts (Noctor et al., 2000). For cellular activity, i.e. of enzymes or transcription factors, while redox homeostasis and redox metabolism, the nature of signalling refers to any transport of information from one a particular antioxidant employed in a specific detoxifica- site to another via a signalling molecule that, by itself, tion reaction and, within limits, the relative redox state of an Chloroplast redox regulation 1451 individual antioxidant may be of minor importance. How- Sensing the cellular redox poise ever, deviations from redox normality can serve in signal Compelling experimental evidence for redox regulation of generation and signal transmission. nuclear gene expression is available for redox signalling induced by the application of ROS, ROS-inducing stress- Defining redox signals in the context of ors, low availability of antioxidants, and by antioxidant photosynthesis feeding, respectively. The common feature of all these treatments is that the cytosolic redox environment speci- The nature of the redox signals perceived, the sensory fically or generally is shifted to a more oxidized or reduced systems, and the classification of the respective responses have received increasing attention in recent years. In plant state. In the context of signal transmission, special attention biology special focus has been given to redox signal has been given to H2O2 (Desikan et al., 2001; Mittler et al., transduction in chloroplasts as well as between chloro- 2004; Vandenabeele et al., 2004). Alternatively, monitor- plasts and the nucleus for experimental and thematic ing the cellular redox environment by sensing the redox reasons. (i) The metabolic state of chloroplast metabolism state of certain metabolites, for example, glutathione and can easily be manipulated by altering exogenous param- ascorbate, has been postulated (Foyer et al., 1997; Dietz, 2003; Pastori et al., 2003; Ball et al., 2004). Both types of eters such as light, CO2, and temperature. (ii) Tools such as chlorophyll a fluorescence-based technology to estimate metabolites, ROS and low-molecular-weight antioxidants, photosynthetic efficiency and redox state, methods at closely interfere. Consequently, in most experiments it is virtually all levels of molecular biology and biochemistry, hardly possible to distinguish between signalling that is and a vast accumulated body of knowledge on structure, possibly originating from H2O2 and that from shifts in the function, regulation, and assembly facilitate interpretation redox poise of low-molecular-weight antioxidants. There- of the results. (iii) Photosynthesis exerts a strong impact fore, they are discussed here together. on the cellular redox signature and nuclear gene expres- Recently cDNA array hybridization experiments were sion and regulates the photosynthetic capacity during long- performed and indicate a strong regulatory function of term adaptation (Dietz, 2003). However, the hypothesis, redox signals on nuclear gene expression. For example, on retrograde redox signalling originating inside chloro- Desikan et al. (2001) analysed the response of Arabidopsis plasts, is generally accepted and despite these systematic thaliana to H2O2 application and Mahalingham et al. advantages, the precise nature of the signals, their speci- (2003) to ozone. Pastori et al. (2003) investigated the regu- ficity and interaction are only recently becoming tangible. lation of transcript amounts in the low-ascorbate mutant Theoretical considerations and experimental data have vtc1 and Vandenabeele et al. (2004) that in a catalase- produced a long list of potential signals, of which a selection deficient tobacco line, as well as Davletova et al. (2005) is discussed here in the context of the regulation of genes that of a knock-out mutant of cytosolic ascorbate peroxi- involved in the control of the cellular redox poise. Due to dase APx1, and Ball et al. (2004) determined the transcrip- the complexity of the possible chemical nature and origin of tional response of the allelic glutathione biosynthetic the signals, defining redox signals depends on the line of mutants rax1-1 and cad2-1. Typical target genes with vision and the intention. For example, Dietz (2003) grouped altered transcript accumulation upon treatment or in the redox signals based on their origin and mode of action in mutants are those for PR proteins, e.g. PR1 (At2g14610), signal transmission. According to his definition, type-I chitinase (At2g43570), and PAL (encoding phenylalanine signals derive specifically from single pathways, while ammonium lyase; At3g53260; At5g04230), and antioxi- type-II signals integrate redox information from various dant enzymes as peroxidases (e.g. At4g11290 and pathways; type-III redox signals indicate more extreme At4g21960), dehydroascorbate reductase (At1g19570) redox imbalances and their transmission depends on cross- and CuZn-superoxide dismutase (At5g18100). The sets of talk with other signalling cascades. Other definitions for target genes widely overlap with the transcripts induced by redox signals are based on the threshold of induction relative pathogens and wounding (Mahalingam et al., 2003; to photosynthetic electron pressure (Pfannschmidt et al., Cheong et al., 2002). 2001a) or on their putative initiation sites (Pfannschmidt The transcription factors involved in these responses were et al., 2003). For chloroplast-to-nucleus signalling, which tentatively identified either by being up-regulated at the depends on passing the chloroplast envelope, a classification transcriptional level (Mahalingam et al., 2003; Pastori based on the chemical nature of the signalling compound et al., 2003; Ball et al., 2004; Davletova et al., 2005) or leaving the chloroplast has been proposed (Baier and Dietz, through the bioinformatic comparison of promoters for 1998). Based on this chemical classification, a concept is stress-induced transcripts (Chen et al., 2002). Candidate followed here in which signals transmitted by redox shifts in transcription factors are WRKY (W-box: TTGACY; cellular redox components or by ROS are distinguished Euglem et al., 2000), WRKY-like (BBWGACYT; Chen from signals transmitted by second messengers synthesized et al., 2002), SA (ACGTCA; Lebel et al., 1998), b-ZIP of inside chloroplasts (Fig. 1). the TGA1-type (TGACG; Schindler et al., 1992), GBF-type 1452 Baier and Dietz (CACGTG; Schindler et al., 1992) and ABRE-type glutathione (Karpinski et al., 1997; Ball et al., 2004). (BACGTGKM; Shinozaki and Yamaguchi-Shinozaki, Consistently, inhibition of PET by DCMU (Karpinski 2000), Myb (AtMyb1: MTCCWACC; AtMyb2: TAACS- et al., 1997) and (over-) expression of catalase or ascorbate GTT; AtMyb3: TAACTAAC; AtMyb4: AMCWAMC; peroxidase in chloroplasts (Yabuta et al., 2004) suppress Martin and Paz-Ares, 1997; Rushton and Somssich, 1998), the high-light-dependent induction of apx2. Constitutive and AP2-like transcription factors (GCCGCC for GCC-box expression of apx2 in the rax1-1 mutant, which is affected binding AP2s or DRCCGACNW for DRE-binding AP2s; in chloroplast glutathione biosynthesis by decreased c- Shinozaki and Yamaguchi-Shinozaki, 2000). glutamyl cysteine synthetase activity (Ball et al., 2004), In response to the many stressors inducing shifts in the also points at signal initiation depending on oxidative cellular redox poise, for example, wounding, pathogens, stimuli. Transcripts for cytosolic APx2 accumulated in ozone, UV-B, and cadmium application, mitogen activated parallel to a decrease in the photochemical quench (qP), protein kinases (MAPK) play a critical role in signal prior to the accumulation of H2O2, and responded differ- transduction (Cheong et al., 2002; Holley et al., 2003; entially to DCMU and DBMIB, which block PET before Yeh et al., 2004). Specifically, MPK3, MPK4, and MPK6 and after the PQ pool, respectively. Therefore, Yabuta et al. are activated by various abiotic stresses (Ichimura et al., (2004) reinstated the hypothesis, originally presented by 2000; Kovtun et al., 2000) making them candidates for Karpinski et al. (1997), that a redox change in PET, signal transduction in redox regulated stress signalling. presumably the redox state of the plastoquinone pool, Upstream in signal transduction, the MAPKs, MPK3 and controls nuclear expression of cytosolic APx2. MPK6, which are activated by the MAPKKs, MKK4 and Apx2 is regulated by a heat shock factor, namely HSF3 MKK5 (Asai et al., 2002) and the MAPKKK ANP1 (Panchuk et al., 2002). In the regulation of apx1, which is (Kovtun et al., 2000), interact with the nucleotide diphos- also H2O2-responsive, the heat-shock factor HSF21 is phate kinase AtNDPK2 in Arabidopsis thaliana. By stimu- involved in H2O2-sensing (Davletova et al., 2005). lation of the phosphorylation activity of MPK3 AtNDPK2 HSF21 transmits the redox signal to the zinc-finger provides enhanced tolerance to multiple stress responses protein Zat12 (Rizhsky et al., 2004), whose expression is (Moon et al., 2003). The MAPK signalling cascades, which under the control of HSF21 (Davletova et al., 2005). resemble animal redox signal transduction pathways Results from apx1 knock-out mutants of Arabidopsis (Halliwell and Gutteridge, 1999), are subjected to an thaliana suggests that cytosolic ascorbate peroxidase ac- additional redox modulation by redox regulation of antag- tivity is involved in signal transmission in excess light, onistic phosphatase activities (Mittler et al., 2004). including ROS-based signal transmission between the In addition to MAPK signalling, thiol-disulphide tran- chloroplasts and the nucleus (Davletova et al., 2005). The sitions can control gene expression in response to ROS sensitivity of ascorbate peroxidases to inhibition by ROS accumulation and changes in the cellular thiol homeo- (Miyake and Asada, 1996), may facilitate signal trans- stasis. By switching of the DNA-binding activity or the mission by micro-bursts. nuclear-cytoplasmic distribution of transcription factors, gene For the regulation of nuclear-encoded chloroplast anti- activity can directly be redox regulated (Sun and Oberley, oxidant enzymes, transcriptome analysis (Kimura et al., 1996). Indications for target thiols are the cysteine 2003; Davletova et al., 2005), the analysis of transcript residues in the C2H2-domains of WRKYs (Maeo et al., amount for the regulation of chloroplast ascorbate perox- 2001) and Cys-260 and Cys-266 in TGA1 whose oxidation idase (Yoshimura et al., 2000), the chloroplast peroxire- prevents binding of the transcription activator protein doxins (Baier and Dietz, 1997; Horling et al., 2003), NPR1 (NON-REPRESSOR OF PR GENES) (Despre´s chloroplast superoxide dismutases (csd2, fsd1; Kliebenstein et al., 2003). et al., 1998), and glutathione peroxidase gpx1 (Milla et al., However, in chloroplast-to-nucleus signalling, a redox 2003) revealed a lower sensitivity of gene expression to signalling pathway triggered by redox imbalances in the shifts in the cytosolic redox poise compared with non- cytosol may only occur under severe oxidative stress. plastidic antioxidant enzymes. However, in 2-Cys peroxi- Under physiological conditions, the availability of reduc- redoxin antisense lines of Arabidopsis thaliana, in which tion energy in conjunction with antioxidant enzymes will a specific component of the chloroplast enzymatic redox maintain the reducing state of the cytosol and quench ROS defence was suppressed, the transcripts of chloroplast signals (Fig. 1). The role of chloroplast metabolism, monodehydroascorbate reductase and stromal and thyla- particularly of photosynthesis, in ROS and antioxidant- koid ascorbate peroxidase were selectively induced (Baier dependent redox regulation has been most intensely studied et al., 2000). Loss of 2-Cys peroxiredoxin function led to for the transcriptional control of the cytosolic ascorbate slight photoinhibition, damage of the photosynthetic mem- peroxidase apx2. In excess light, the apx2 promoter is brane, and oxidation of the ascorbate pool, suggesting strongly stimulated (Karpinski et al., 1997), presumably by photo-oxidative stress (Baier and Dietz, 1999b). The fact the light-induced accumulation of H2O2 (Chang et al., that three transcripts for chloroplast antioxidants accumu- 2004) and/or a decrease in the reduction state of leaf lated, while the transcript levels for various other antioxidant Chloroplast redox regulation 1453 enzymes did not respond, indicates chloroplast-specific Characterization of the mutant ulf3, which is allelic to gun2 signals triggering nuclear expression (Baier et al., 2000). (Susek et al., 1993), demonstrated that tetrapyrrole bio- synthesis is concurrently regulated by FLU mediating the feedback from the Mg2+ branch and ulf3/gun2 controlling Chloroplast-to-nucleus redox signals for the haem branch (Goslings et al., 2004), which makes transmission of moderate redox imbalances tetrapyrroles unlikely to accumulate in mature tissues. In addition, Keetman et al. (2002) showed, in tobacco Efficient transmission of a signal depends on a low thresh- coproporphyrinogen oxidase antisense lines, which accu- old concentration. Accumulation of the signal, in turn, is mulate protoporphyrin-IX, that imbalances in tetrapyrrole controlled by its stability within the metabolic network. biosynthesis primarily lead to modulation of gene expres- Therefore, messengers that are metabolically more inert and sion by photosensitization of the pigments. Redox signals, cannot or can only slowly be inactivated are more efficient for example, H2O2 accumulation or shifts in the redox state than redox compounds such as ROS and oxidized antioxi- of low-molecular-weight antioxidants, may be involved in dants that are decomposed or reduced, respectively, during the suppression of nuclear gene expression in norflurazone- diffusion through the cell. In respect of chloroplast-to- treated seedlings, although Strand et al. (2003) excluded nucleus signalling, several putative signals have been severe differences in the steady-state levels of superoxide suggested, of which some will be discussed here. for the gun mutants by semi-quantitative NBT-staining. In mature leaves, expression of cab3, which was used as Tetrapyrrole signals a target gene in the gun-screen, is regulated by photosyn- Indications for tetrapyrrole signals come from the analysis thetic electron transport (Sullivan and Gray, 2002), pre- of cab gene expression during de-etiolation of Arabidopsis sumably by the acceptor availability of photosystem I seedlings (Susek et al., 1993). The arrest of chloroplast (Pursiheimo et al., 2001). Photo-damaged tetrapyrroles development by a norflurazone-mediated block of caroten- may regulate nuclear gene expression, as for example, oid biosynthesis suppressed the expression of various photo-oxidized haem controls the capping of catalase nuclear-encoded chloroplast proteins, for example, Lhcb1, mRNA in rye (Schmidt et al., 2002). PsbR, RbcS, PetH, and PetE, during early seedling de- velopment (Harpster et al., 1984; Mayfield and Taylor, 1984; Bolle et al., 1994; Gray et al., 1995). Based on these Oxolipin signals observations, retrograde chloroplast signals were hypothe- Besides oxidatively damaged tetrapyrroles, oxolipins are sized for the control of nuclear transcription (Taylor, 1989). another type of putative redox-related signals in chloroplast- A first insight into signalling was provided by Susek et al. dependent redox regulation. In pathogen response, for (1993), who isolated Arabidopsis mutants (gun), that example, they modulate oxidative bursts (Rao et al., 2000). express cab3, encoding Lhcb1-2, although chloroplast Their biosynthesis initiates from alkyl hydroperoxides, development had been arrested by norflurazone. Mapping which are formed preferentially under unfavourable con- of the mutations showed defects in haem oxidase (gun2), ditions by oxidation of unsaturated fatty acids either phytochromobilin synthase (gun3), a regulator of Mg- mediated by ROS (Ble´e and Joyard, 1996), lipoxygenase chelatase (gun4), and the H-subunit of Mg-chelatase (LOX) (Feussner and Wasternack, 2002) or fatty acid (gun5) (Mochizoki et al., 2001; Larkin et al., 2003; Strand dioxygenases (DOX) (de Leon et al., 2002). Detailed et al., 2003) indicating a role of tetrapyrrole biosynthesis in time-resolved mass spectrometric analysis of lipids and the regulation of nuclear transcription (Strand et al., 2003). lipid hydroperoxides (Montillet et al., 2004) revealed early Either Mg-protoporphyrin-IX, haem or a haem precursor activation of the 13-LOX pathway in response to various were assumed to be released from chloroplasts and to kinds of stresses. By contrast, ROS-mediated peroxidation, modify nuclear gene expression by binding to a regulatory which is stimulated by excess excitation energy, appears to protein, which interacts with the CUF1-element found in be a late process (Montillet et al., 2004) when the antioxi- several promoters of 70 genes mis-regulated in gun2 and dant defence is close to oxidative collapse. Various plant gun5 (Strand et al., 2003; Strand, 2004). signalling molecules are synthesized from alkyl hydroper- In higher plants, the pathways of chlorophyll and haem oxides (Ble´e and Joyard, 1996). Jasmonates, which are biosynthesis are tightly regulated at an early step. Haem a group of 12-carbon fatty acid cyclopentanones and dinor- triggers feed-back inhibition of Glu-tRNA reductase, which oxo-phytodienoic acids, and 2(R)-hydroperoxide fatty catalyses biosynthesis of the tetrapyrrole precursor d- acids, and are well known from pathogen and wounding aminolevulinic acid (ALA) (Beale, 1999). While haem responses, protect plant cells from oxidative stress and cell binds to the N-terminus of the enzyme (Vothknecht et al., death (Farmer et al., 1998; Mauch et al., 2001; Hamberg 1998), FLU, which is a negative regulator of chlorophyll et al., 2003). biosynthesis (Meskauskien et al., 2001), regulates Glu- Inside the chloroplast, accumulation of lipid peroxides is tRNA reductase at the C-terminus (Goslings et al., 2004). suppressed by glutathione peroxidases and peroxiredoxins. 1454 Baier and Dietz Both enzymes are haem-free peroxidases reducing alkyl Photosynthetically controlled signals hydroperoxides by a thiol-based reaction mechanism (Baier The redox state of the plastoquinone pool: Efficient regula- and Dietz, 1999a). The genome of Arabidopsis thaliana tion of gene expression in relation to photosynthesis should contains two open reading frames for chloroplast glutathi- directly respond to photosynthetic activity. In recent years, one peroxidases (gpx1 and gpx7), of which only gpx1 is photosynthetic control of both nuclear as well as plastid expressed (Milla et al., 2003), and four open reading frames gene expression has been linked to the redox state of the for chloroplast peroxiredoxins (Horling et al., 2003). plastoquinone (PQ) pool which regulates expression of, for Peroxiredoxins and gpx1 are induced by H2O2 and butyl- instance, petE2 (Pfannschmidt et al., 2001b), encoding a hydroperoxide (Horling et al., 2003; Avsian-Kretchmer plastocyanin, in sugar-starved cells (Oswald et al., 2001) et al., 2004) indicating that their expression possibly and under low light conditions (Pfannschmidt et al., antagonizes oxolipin signal formation. However, expres- 2001b). A small pool of 7–10 PQ molecules per photosys- sion of gpx1 and 2CPA, which are the only isogenes for tem II mediates electron transfer between photosystem II which the analysis has been performed so far, are not and the cytochrome b6 f-complex, making plastoquinol responsive to jasmonates or salicylates (Milla et al., 2003; diffusion the rate limiting step (Haehnel et al., 1984). The Baier et al., 2004) suggesting primary control of oxolipin relative activities of photosystem II as electron input and biosynthesis by the relative rates of fatty acid peroxidation. photosystem I as drainage, cyclic electron transport and Peroxide formation and reduction may be further uncoupled chlororespiration adjust the redox state of PQ (Allen, 1992; due to the sensitivity of the active site cysteine residues to Heber, 2002). Depending on the PQ redox state presum- over-oxidation. 2-Cys Prx have been suggested to func- ably by binding of plastoquinol to the cytochrome b f- tion as flood gates that normally keep peroxides at a low 6 complex (Zito et al., 1999), the kinase TAK1 is activated level (Wood et al., 2003; Ko¨nig et al., 2003). Following and initiates processes like state transition (Snyders and a sudden increase in peroxides they are over-oxidized and Kohorn, 2001). Whether this kinase also transmits other inactivated. Subsequently, the oxolipin signal can spread kinds of PQ-dependent responses, for example, in the freely as shown for mammalian cells (Wood et al., 2003). regulation of psaAB transcription (Pfannschmidt et al., Glutathione peroxidases, which show only low activities in plant cells, and the ascorbate peroxidases, which are 1999) and nuclear expression of petE2, or whether PQ triggers several independent signal transduction cascades in highly specific for H2O2 and sensitive to inactivation by low ascorbate availability, are very likely not able to parallel is still open for discussion. compensate for decreased Prx activity. Plant 2-Cys Prx is Regarding expression of other nuclear-encoded chloro- efficiently inactivated especially by bulky peroxides, like plast proteins, co-regulation with the redox state of the PQ lipid peroxides (Ko¨nig et al., 2003). Therefore, with the pool has been demonstrated for cab genes in unicellular accumulation of alkyl hydroperoxides, oxolipin biosyn- green algae (Escoubas et al., 1995; Maxwell et al., 1995). thesis may get increasingly dependent on LOX-, DOX-, A more detailed recent study (Chen et al., 2004) demon- and ROS-stimulation. strates that, in the case of Dunaliella tertiolecta, PQ- In recent years various mutants with decreased sensitiv- dependent modulation of lhcb1 expression starts only 8 h ity to jasmonates (and salicylates) and high sensitivity to after modifying the PQ redox state. Immediately after ROS have been isolated, for example, the jin (Berger et al., inducing the redox shift in the PQ pool the trans-thylakoid 1996), jar (Staswick et al., 2002), coi1 (Xie et al., 1998), membrane potential is the predominant regulator of gene npr1 (Scott et al., 2004), rcd1 (Ahlfors et al., 2004), and oji expression. The long lag phase suggests that expression of mutants (Kanna et al., 2003). Although primarily investi- signal transduction elements and proteins involved in the gated in relation to the wounding and pathogen response, co-ordination of a regulatory network is necessary for the signal transduction elements identified could also be establishing the correlation between gene activity and the involved in any other type of oxolipin signalling, such as in redox state of the PQ pool. the chloroplast-to-nucleus signalling discussed here. The In higher plants, only weak indication for PQ-dependent first components of jasmonate signal transduction have regulation of genes for light-harvesting complex proteins been cloned: Jin1, which is essential for discrimination (LHCP) is available. For cab genes, encoding LHCP of between different jasmonate-regulated defence responses, photosystem II, PQ-dependent regulation has been experi- encodes the transcription factor AtMyc2 (Lorenzo et al., mentally excluded for winter rye by Pursiheimo et al. 2004), the F-box protein COI1 with 16 leucine rich motifs (2001), who describe a correlation of gene expression with (Xie et al., 1998), and the WWE-protein RCD1 (Ahlfors the acceptor availability of photosystem I. In addition, PQ- et al., 2004). Recent cloning of JAR1, which encodes dependent redox regulation was not observed for nuclear a jasmonate amino acid synthetase, showed that jasmonates encoded psaF and psaD expression in mustard seedlings are activated by conjugation to isoleucine (Staswick and (Pfannschmidt et al., 2001b). Interestingly, even in the case Tiryaki, 2004) which is another chloroplast-derived of petE2, which to date is the model gene for the regulation metabolite. of nuclear gene expression by the PQ redox state, other Chloroplast redox regulation 1455 signals such as the sugar status (Oswald et al., 2001), the release of reduction energy into the cytosol, the phytochrome-A (Dijkwel et al., 1997) and abscisic acid chloroplast peroxidase activity and chloroplast translation (Huijser et al., 2000) are dominant regulators in Arabidopsis (Schu¨rmann, 2003; Ko¨nig et al., 2002; Barnes and May- thaliana. In pea and tobacco, PQ-dependent regulation is field, 2003). As indicated by the spectrum of target proteins overwritten and antagonized post-translationally by a PET- (Motohashi et al., 2001), redox regulation depending on the dependent signal (Sullivan and Gray, 2002). It is tempting to redox state of thioredoxins is manifold and far from being assume that the PQ signal, which is central in regulating state understood comprehensively. In this context, the classifi- transition (Allen, 1992) and chloroplast transcription of cation of Trx function as signal, sensor or transmitter of photoreaction centre proteins (Pfannschmidt et al., 1999), is redox information depends on definition. The reduction of minor importance for chloroplast-to-nucleus signalling in state of thioredoxin is an indicator of redox state and thus mature leaves and under most environmental circumstances. a transmitter for subsequent signal generation by down- According to the gradual model of redox signalling proposed stream events rather than the signal or sensor itself. The by Pfannschmidt et al. (2001a) PQ triggers the signalling sink capacity for consumption of reduction energy of the pathway with the highest sensitivity and lowest threshold thiol system is determined by the auto-oxidation rate of to redox imbalances. Based on the data available, PQ- target proteins (Schu¨rmann, 2003) and, in case of peroxi- dependent signalling appears to have an ancillary or redoxins, by the rates of peroxide reduction (Ko¨nig et al., insignificant role in controlling the genetic responses to 2002). Electron drainage into the thioredoxin pathways metabolically relevant redox imbalances in green tissues withdraws electron from ferredoxin:NADP+-reductase and under ambient growth conditions and moderate stress. This the Mehler reaction (Fridlyand and Scheibe, 1999) and thus conclusion is supported by a recent study in which regulation competes with the generation of ROS and possible (re- of gene expression in response to PQ redox state has been ductive) signals in metabolic pathways. The allocation of studied on a transcriptome level (Fey et al., 2005). Although electrons between the different metabolic sinks has to be small sets of genes have been identified as being responsive adjusted for optimal assimilation rate versus dissipation of to the PQ redox state, the experiments were performed at excess energy. For example, peroxides produced in the photon flux densities of less than 40 lmol mÿ2 sÿ1, i.e. Mehler reaction are detoxified by ascorbate peroxidase or conditions that barely have major relevance for regulatory peroxiredoxin yielding dehydroascorbic acid and oxidized adjustment of photosynthesis under natural conditions. peroxiredoxin, respectively. Through the regeneration of At higher light intensities (a cloudy day corresponds to reduced ascorbate and peroxiredoxin, both reaction se- 100–300 lmol mÿ2 sÿ1and a sunny day to 1500–2000 lmol quences consume further reductive power and relieve mÿ2 sÿ1) the PQ pool is intermediately reduced under most electron pressure in the PET chain (Fortis and Elli, 1996; conditions. However, in the vascular tissues and their bundle Dietz et al., 2002). Redox information must be central in sheaths, where the redox state of the PQ pool may be the regulation of these processes. controlled more strongly by NADPH-dependent, presum- ably NDH-mediated reduction (Peltier and Cournac, 2002), Photosynthates and the plastidic redox state of NADPH/ a signalling function is more likely. Therefore, expression of NADP+: The photosynthetic electron transport drives re- cytosolic apx2, which is preferentially expressed along the ductive metabolism. Therefore, basically any metabolite main veins (Ball et al., 2004), may correlate with the PQ synthesized, depending on the availability of reducing redox state (Yabuta et al., 2004) as well as with the cellular energy, could be a redox signal. Examples for putative redox status (Chang et al., 2004) and the availability of low signalling metabolites are carbohydrates (‘sugar sensing’), molecular weight antioxidants (Ball et al., 2004). which are synthesized in photosynthesis and consumed in mitochondria by respiration depending on the cellular Thioredoxin-mediated signals: At the acceptor site of photo- energy status (‘energy sensing’). Channelling reduction system I, ferredoxin-thioredoxin reductase reduces thio- energy between chloroplasts and mitochondria can protect redoxins (Trx) depending on the electron pressure and the photosynthesis against photoinhibition (Saradadevi and reduction state of ferredoxin (Fridlyand and Scheibe, 1999). Raghavendra, 1992). In light-enhanced dark respiration, A genome-wide survey showed various chloroplast thio- malate is the preferred redox transmitter (Padmasree et al., redoxins, namely four Trx-m, two Trx-f, two Trx-y, and one 2002). NADH generated by dehydrogenase activity is Trx-x (Collin et al., 2004). Together with other small redox fed into the respiratory electron transport chain and the proteins like glutaredoxins (Rouhier et al., 2004) and alternative oxidase branch (Gardestro¨m et al., 2002). It is cyclophilins (Romano et al., 2004) they mediate thiol- open for debate if and how sensing of the cytosolic disulphide redox interchange of various chloroplast pro- carbohydrate concentration interferes with redox signalling. teins like fructose-1,6-bisphosphase, malate dehydrogenase, Sugar signalling involves, for example, hexokinase (Jang peroxiredoxins, and the RB60-protein with partly over- et al., 1997), which drives the expression of various lapping specificity. The redox states of the target proteins nuclear-encoded chloroplast proteins, including suppres- modulate the chloroplast metabolite fluxes, ATP synthesis, sion of Rubisco, light-harvesting complex proteins, and 1456 Baier and Dietz seduheptulose bisphosphatase (Moore et al., 2003), and regulation by the redox state of chloroplast NADPH/ SNF1-like kinases (Halford et al., 2003). Some of the target NADP+ (Pursiheimo et al., 2001; Baier et al., 2004). genes, for example, lhcb1 (cab3) and petE2, are also model However, transcriptional activity of cab genes and 2CPA genes in the analysis of redox signalling (see above). In is distinctly regulated in response to photosynthates. While addition to stimulating respiration, carbohydrate fluxes transcription of lhcb1 is suppressed by sugars via the between chloroplast and cytosol mediate the exchange of hexokinase-dependent pathway (Moore et al., 2003), information on the chloroplast redox state. Two well- regulation of 2CPA is independent of sugar signalling studied examples for redox valves controlled by carbohy- (Baier et al., 2004). Low concentrations of externally drate metabolism are the malate-oxaloacetate shuttle and applied sugars even increases 2CPA promoter activity by the triose phosphate/3-phosphoglycerate shuttle (Heineke 10–20%. The dominance of redox-regulation of 2CPA was et al., 1991) (Fig. 2). Both transporters exchange redox demonstrated by low 2CPA-promoter driven reporter gene energy between the chloroplastic NADPH and the cytosolic activity in the presence of strong electron sinks such as + ÿ NADH-system. Since the chloroplastic NADPH/NADP CO2 and NO3 (Baier et al., 2004). Since the inhibition of ratio is about 0.5 in the light and the cytosolic NADH/ PET also decreased the promoter activity, regulation NAD+ ratio about 10ÿ3 (Heineke et al., 1991), the transport depends on photosynthetic activity. Apparently, the ac- is essentially unidirectional due to photosynthetic activity ceptor availability of photosystem I, possibly mediated by and depends on the photosynthetic electron pressure the redox state of the NADPH/NADP+-system, controls (triose-phosphate/3-phosphoglycerate shuttle) and Trx- the promoter activity (Baier et al., 2004). dependent enzyme activation (malate valve). External application of millimolar amounts of peroxides Other putative signalling molecules are amino acids, only slightly increased 2CPA transcript amount (Baier and whose biosynthesis provides a strong electron sink by the Dietz, 1997; Horling et al., 2003; Baier et al., 2004), high consumption of reduction energy in carbohydrate while a strong up-regulation was seen upon wounding biosynthesis and nitrate reduction. That the signalling path- which rapidly and efficiently suppresses photosynthetic ways, which are presently under investigation (Palenchar activity (Chang et al., 2004). These data support the view et al., 2004), could have an impact on chloroplast redox that the regulatory redox signal is of chloroplast origin. signature is, for example, indicated by co-regulation of the Pharmacological studies suggest that signal transduction ferredoxin gene At2g27510 and the two ferredoxin-NADP+- takes place via protein kinases. In the expressional reductases At1g30510 and At4g05390. Expression of the inhibition under reducing conditions a staurosporine- proteins, which are involved in distributing electrons from sensitive serine/threonine kinase is involved, while under the photosynthetic light chain to NADP+, is controlled by oxidizing conditions a PD98059-sensitive MAPKK trans- a carbon/nitrogen signalling pathway with dominance of the mits the signal (Horling et al., 2001; Baier et al., 2004). carbon component (Palenchar et al., 2004). The analysis of Arabidopsis mutants with lower induction Analyses of lhcb1 transcription in winter rye and of of 2CPA, the rimb-mutants, suggests that chloroplast 2-Cys Prx (2CPA)inArabidopsis thaliana indicate monodehydroascorbate reductase, stromal ascorbate per- oxidase, chloroplast CuZn superoxide dismutase csd2, and plastidic malate dehydrogenase are modulated by components of the signalling pathway triggering 2CPA expression (I Heiber and M Baier, unpublished results).

Abscisic acid and violaxanthin-cycle activity: In case of 2CPA gene expression, redox regulation of transcription depends on the plant hormone abscisic acid (ABA) (Baier et al., 2004). In addition, ABA-responsive cis-elements are found in promoters of many nuclear-encoded chloroplast proteins (Weatherwax et al., 1996; Milla et al., 2003). The close interrelation between ABA signalling and photosyn- thesis is indicated by the isolation of alleles for ABA- biosynthetic enzymes and for ABA signal transduction elements in screens for mutants impaired in the expression of the plastocyanin gene petE2 (Huijser et al., 2000) and Fig. 2. The malate-oxaloacetate and the triose-phosphate-shuttle link the gene for a regulatory subunit of ADP-glucose pyro- the chloroplast NADPH pool with the cytosolic NADH-pool. 3-PGA, phosphorylase (apL3; Rook et al., 2001). PetE2 (Huijser 3-phosphoglycerate; 1,3-bPGA, glycerate-1,3-bisphosphate; DHAP, di- et al., 2000) is like 2CPA (Baier et al., 2004) suppressed by hydroxyacetonephosphate; GAP, glyceraldehyde-3-phosphate (figure adapted from Heineke et al., 1991. ªThe American Society of Plant ABA, while apL3 (Rook et al., 2001) is like apx2 (Chang Biologists, with permission). et al., 2004) ABA-induced (Fig. 3). Chloroplast redox regulation 1457

thylakoid lumen thylakoid chloroplast stroma cytosol

NCED Asc H+ neoxanthin xanthoxin xanthoxin

AscH violaxanthin + NADP ABA aldehyde VDE antheraxanthin ZE NADPH DHA zeaxanthin NADPH ABA PS-I H+ + + NADP Transcription H + O2 ROS ROS PS-II Asc DHA apx2, apL3 H2O

NADP+ DHA DHA GSH 2CPA, petE2

Asc Asc GSSG NADPH

Fig. 3. Regulation of ABA biosynthesis by photosynthesis. Violaxanthin de-epoxidase (VDE) acitivity is stimulated by thylakoid acidification and driven by the availability of protonated, reduced ascorbate (AscH), while zeaxanthin epoxidase (ZE) depends on NADPH. Under photo-oxidizing conditions, detoxification of ROS can limit VDE due to increased oxidation of ascorbate (Asc) to dehydroascorbate (DHA). 9-cis-epoxycarotenoid dioxygenase (NCED) catalyses xanthoxin synthesis from neoxanthin and violaxanthin. In the cytosol ABA is synthesized in two steps from xanthoxin and regulates nuclear gene expression by triggering a specific signalling cascade.

ABA biosynthesis starts inside the chloroplast and membrane (Foyer and Lelandais, 1996). The supply with depends on xanthoxin synthesized from violaxanthin reduced ascorbate to the lumen is affected by the local and the violaxanthin-derivative neoxanthin (Finkelstein redox poise on the stromal site, where, for example, the and Rock, 2002) (Fig. 3). Most of the violaxanthin within Mehler reaction and ascorbate peroxidase activity strain the thylakoid membrane takes part in the xanthophyll cycle, the ascorbate pool. The redox regulation of ABA which is a redox reaction system of reversible xanthophyll biosynthesis dependent on PET is further enhanced by epoxidation and de-epoxidation (Eskling et al., 1997). In redox-regulation of ABA signal transduction, as oxidative excess light, the xanthophyll cycle is activated for the inhibition of the ABA antagonistic phosphatases ABI1 dissipation of excess energy. De-epoxidation of violaxan- and ABA2 (Meinhard and Grill, 2001; Meinhard et al., thin to zeaxanthin via antheraxanthin requires reduced and 2002) increases ABA sensitivity. protonated ascorbic acid in the thylakoid lumen (Bratt The oxidative stimulation of ABA biosynthesis and et al., 1995), which makes it not only dependent on the ABA signal transduction has a different impact on the ascorbate content, but also on the redox state of the expression of various antioxidant enzymes. For example, ascorbate pool. Regeneration of ascorbate is covered by transcript levels of cytosolic ascorbate peroxidase apx2 are the NADPH-dependent Halliwell–Foyer cycle (Foyer and up-regulated by ABA (Cheong et al., 2004). As a conse- Halliwell, 1977). However, if dehydroascorbate reduction quence of ABA-induced H2O2 generation, apx2 is induced cannot keep pace with ascorbate oxidation, the xanthophyll under photoinhibitory conditions (Chang et al., 2004). cycle gets uncoupled. If violaxanthin accumulates, it may High activity of the antioxidant enzyme helps to balance the promote ABA synthesis. The hypothesis on the regulation cytosolic redox poise, as long as the cytosolic ascorbate of ABA-biosynthesis by ascorbate availability is supported availability is sufficient to support H2O2 reduction. Thus, it by the characterization of the ascorbate biosynthetic mutant is assumed that the chloroplast ABA signal synergistic- vtc1 (Pastori et al., 2003). In leaves, which accumulate only ally increases the cytosolic antioxidant capacity before 30% of wild-type ascorbate (Conklin et al., 1997), the ABA the extraplastidic compartments are flooded with photo- content was increased by 60% (Pastori et al., 2003). In oxidatively produced ROS. In addition to cytosolic apx2 parallel, the expression of 9-cis-epoxycarotenoid dioxygen- (Chang et al., 2004), chloroplastic gpx1 is induced by ABA ase (NCED) increased (Pastori et al., 2003), which catal- (Milla et al., 2003). GPx1 acts independently of ascor- yses the irreversible oxidative cleavage of neoxanthin and/ bate by using reduced glutathione as a co-factor, which or violaxanthin to xanthoxin (Finkelstein and Rock, 2002), can more efficiently be regenerated inside the chloroplast indicating that ABA biosynthesis in a low ascorbate by glutathione reductase at the expense of NADPH (Baier background is also promoted by the adaptation of gene et al., 2000; Noctor et al., 2000). Under photoinhibitory expression. conditions, increased amounts of Gpx1 may substitute The thylakoid lumen is especially sensitive to limita- for chloroplast ascorbate peroxidase, which is susceptible tions in ascorbate availability since it depends on non- to shifts in the redox poise of ascorbate (Miyake and catalysed diffusion of ascorbate through the thylakoid Asada, 1996). 1458 Baier and Dietz Expression of 2CPA, which is a peroxidase reducing a broad range of peroxides independent of low-molecular- gene expression weight antioxidants as co-factors (Baier and Dietz, 1999a, b;Ko¨nig et al., 2003) is suppressed by ABA (Baier et al.,

2004). The antagonism of oxidative induction and ABA NADPH suppression may keep the transcript and protein on fairly ABA nucleus constant, but high, levels under most growth conditions 2-Cys Prx chloroplast ROS including stress situations (Baier and Dietz, 1996, 1997; ROS Horling et al., 2003; Baier et al., 2004). Exceptions are ROOH ROH Oxolipins cytosolic observed under severe stresses like wounding (Baier et al., antioxidant 2004) and limitations in thioredoxin regeneration (Keryer cytosol defence et al., 2004), which is needed for driving peroxiredoxin activity (Ko¨nig et al., 2002). Biochemical analysis of 2-Cys Fig. 4. 2-Cys peroxiredoxins as source and target for redox regulation. Prx in barley (Ko¨nig et al., 2003) demonstrated that under 2-Cys Prx are nuclear encoded chloroplast peroxidases, which reduce alkylhydroperoxide (ROOH). Under photo-oxidative stress conditions, stress conditions increasing portions of the active site of the the active site of the enzyme gets inactivated by over-oxidation. Con- enzyme get over-oxidized. The oxidation causes conform- formational changes lead to decamerization of 2-Cys peroxiredoxin and ational changes leading to decamerization and attachment thylakoid attachment. Gene expression is regulated by the redox poise of NADPH/NADP+, ROS, and abscisic acid (ABA), with increasing amounts of the inactive enzyme to the thylakoid membranes (Ko¨nig of NADPH and ABA repressing the promoter activity and higher oxidation et al., 2003). Ongoing work with transgenic Arabidopsis of the NADPH/NADP+-system and ROS inducing it. The oxolipin thaliana lines and in vitro studies with isolated thylakoids jasmonic acid and salicylic acid, whose biosynthesis can possibly be regulated by 2-Cys Prx-dependent reduction of alkyl hydroperoxides, do and heterologously expressed PRX suggest that the binding not directly influence promoter activity. However, they could, like ABA, of 2-Cys Prx to the thylakoid membrane modulates PET increase the oxidative strain on the cytosolic redox environment. (P Lamkemeyer, WX Li, M Laxa, K-J Dietz, unpublished results). As outlined above, 2CPA expression is antagonis- tically regulated by negative inputs through ABA and reductive stimuli, and positive input by oxidative stimuli. In chloroplasts, antioxidant enzymes came together This mechanism reduces the rates for re-synthesis of active from different evolutionary origins (Asada, 2000). They enzyme under stress conditions (Fig. 4). Another explan- have been adapted for their function in protecting against ation for ABA-dependent suppression of 2CPA may be the risks of oxygenic photosynthesis, while the oxygen linked to its substrate spectrum. Prx reduces a wide range of concentration and light intensities increased. Together alkyl hydroperoxides (Ko¨nig et al., 2002) some of which with the chloroplast targeting signals, the promoters have are precursors for oxolipid biosynthesis (Ble´e and Joyard, evolved. From double targeting of the antioxidant en- 1996). Consistent with the finding by Andersson and co- zymes glutathione reductase, ascorbate peroxidase, and workers (2004) that disruption of AtMYC2, which encodes monodehydroascorbate reductase into chloroplasts and a transcription factor positively regulating ABA-responses, mitochondria (Chew et al., 2003) it has to be assumed resulted in elevated expression of jasmonate responsive that this process is still ongoing. 2-Cys peroxiredoxins genes, ABA-suppression of 2CPA may lead to stimulated and glutathione peroxidase already show compartment- rates of jasmonate synthesis. specific targeting and regulation (Baier and Dietz, 1997; Mullineaux et al., 1998). For 2-Cys peroxiredoxin-A, which is very likely of endosymbiotic origin (Baier and Perspectives Dietz, 1997), by taking over an ancient function in the In the context of photosynthesis and in the regulation of protection of the photosynthetic membrane, promoter antioxidant enzymes, chloroplasts act both as source and adaptation closed a regulatory circuitry of multi-level target of redox regulation. They are tightly integrated in redox regulation, in which the chloroplast enzyme is the cellular metabolism, a fact that often complicates the source and the target of redox regulation (Fig. 4). experimental dissecting of signal transduction pathways Analysis of the gpx gene structures (Milla et al., 2003) and pinpointing the causes and consequences of regulatory points to the multiplication of a single ancestor gene. reactions. During evolution, the endosymbiont maintained Only gpx1 transcripts, which encode the chloroplast its photosynthetic capacity with all the associated potential isoforms, are induced by ABA and gpx1 is, besides oxidative hazards. However, most structural and functional gpx6, the only gpx gene not responding to the oxolipin genes were transferred from the plastome to the nucleus, derivates jasmonic acid and salicylic acid (Milla et al., including all antioxidant and most regulatory genes. A 2003). The regulation pattern indicates specific responses sophisticated network of regulation evolved composed of to second messengers generated by chloroplast metabol- anthero- and retrograde signalling pathways with signifi- ism by moderate (ABA) and strong (oxolipins) redox cant crosstalk and efficient feedback. imbalances. Chloroplast redox regulation 1459 Acknowledgement Ble´e E, Joyard J. 1996. Envelope membranes from spinach chloroplasts are a site of metabolism of PUFA hydroperoxides. 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