photosynthesizing

The redox status of the cell is described by the ratio of reduced to non-reduced compounds. Redox reactions which determine the redox state are an essential feature of all living beings on Earth. However, the first life forms evolved under strongly anoxic conditions of the young Earth, and the redox status probably was based on iron and sulphur compounds. Nowadays, redox reactions in cells have developed in strict connection to molecular oxygen and its derivatives i.e. reactive oxygen species (ROS). Oxygen has started to accumulate on the Earth due to oxygenic photosynthesis. All aspects of aerobic life involve ROS, reactive nitrogen species (RNS), antioxidants and redox regulation. Many different redox-active compounds are involved in the complex of redox processes, including pyridine nucleotides, thioredoxins, glutaredoxins and other thiol/disulphide-containing proteins. Redox regulation is integrated with the redox-reactions in photosynthesis and respiration to achieve an overall energy balance and to maintain a reduced state necessary for the biosynthetic pathways that are reductive in nature. It underlies the physiological and developmental flexibility in plant response to environmental signals.


INTROducTION
Higher plants that dominate in terrestrial ecosystems have evolved multiple adaptive strategies to survive and reproduce in the constantly changing environment with respect to temperature, light, CO 2 , water and nutrient status.Moreover, under natural conditions they suffer from many abiotic and biotic stress factors that usually act in combination, a phenomenon known as multistress (Mittler, 2006).Consequently, plants always respond to a unique complex of growth conditions.Integration of many signals into a comprehensive signalling network to coordinate the regulation of growth and developmental processes under fluctuating environmental conditions is the molecular basis for this flexible response.Advances in our understanding of this mechanism rely on new concepts of oxidative stress and redox signalling commonly attributed to a plant response to environmental constraints.

REdOx STATuS AT THE vERy EARly STAgE Of EvOluTION
Phylogenetic analyses locate the root of the tree in non-photosynthetic microbes (e.g.Pace, 1997;Reysenbach & Shock, 2002;Olson & Blankenship, 2004) just between Bacteria and Archaea domains (Zhaxybayeva et al., 2005), although this question is still the subject of hot debates (e.g.Dagan & Martin, 2006;Di Giulio, 2007;Wong et al., 2007;Mat et al., 2008).Metabolic processes of the pre-photosynthetic biosphere most likely involved energy derived from redox disequilibrium involving Fe, S, C, H 2 and O 2 (Walker, 1977), and early life depended on energy sources provided by redox disequilibria generated by abiotic mass transfer of geological processes (Canfield et al., 2006;Sleep & Bird, 2007).Nowadays almost all life on Earth depends ultimately on photosynthetic primary producers (e.g.Holser et al., 1988), and photosynthesis is an ancient process on Earth (Fig. 1).Some ancestral systems were adapted to photoautotrophic photosynthesis in low redox environments and might well have functioned in phototrophic bacteria that used reduced sulphur compounds as electron donors for CO 2 fixation (Olson & Pierson, 1986).The first photosynthetic processes, a huge metabolic innovation, probably developed from a series of pre-adaptations to the environmental conditions of the pre-photosynthetic niches (Sleep & Bird, 2008).Hydrogen based photosynthesis probably evolved gradually from photocatalysis related to the acetogenesis reaction, which is a form of anoxygenic photosynthesis, and the ability to metabolize iron and sulphur compounds pre-adapted organisms for the use of sulphide and ferric iron as abundant oxygen acceptors.This freed a bacterium from its dependence on redox disequilibrium in geological processes as a source of available energy (Sleep & Bird, 2008).The most ancient form of anoxygenic photosynthesis may well have used external reductants as reduced sulphur compounds or ferrous iron as electron donors for CO 2 fixation (Olson & Pierson, 1986;Olson & Blankenship, 2004).There is no standard term and no convenient candidate for the chemical species that is oxidized during anoxygenic photosynthesis (Sleep & Bird, 2008), but most likely the following reactions were possible at the early stages of life evolution: (e.g.Grassineau et al., 2001) and Ehrenreich & Widdel, 1994;Kappler & Newman, 2004).
Waves, tides, sea spray and storms transported countless photosynthetic microbes from their marine ecosystem onto land.The first Terrabacterium on land faced vicissitudes (Sleep & Bird, 2008).The successful land colonists, Terrabacteria, evolved into ecosystems of photosynthetic organisms and actinobacteria that weathered exposed rock and formed soil.Anoxygenic photosynthetic ecosystems benefited from efficient weathering and the primary producers acquired ferrous iron as an oxygen acceptor (Sleep & Bird, 2008).Subsequently, weathering and diagenetic rock alteration affected the geological evolution of the Earth's crust (Rosing et al., 2006).
The transition from anoxygenic to oxygenic photosynthesis took place when the cyanobacteria "learned" how to use water as an electron donor for carbon dioxide reduction.Before that time hydrogen peroxide (H 2 O 2 ) may have served as a transitional donor, and before that, ferrous iron may have been the original source of reducing power (Olson & Blankenship, 2004).Borda et al. (2001) showed that pyrite-induced hydrogen peroxide formation from H 2 O might well have taken place in the absence of oxygen on the early Earth.Several authors (Bader, 1994;Rutherford & Nitschke, 1996;Samuilov, 1997; see also discussion below) have suggested hydrogen peroxide as an early electron donor to photosystem II (PSII).
Cyanobacteria appeared on land (around 2.5 billion years (Ga) ago (Fig. 1.) Battistuzzi et al., 2004;Sleep & Bird, 2008).Carbon isotope data suggest that autotrophic carbon fixation was taking place at least a billion years earlier (Olson & Blankenship, 2004).However, it is not possible to determine from the biomarkers alone whether these cyanobacterial ancestors actually carried out oxygenic photosynthesis (Olson & Blankenship, 2004).Schopf (1993) and Schopf and Packer (1987) have proposed on the basis of morphology alone that the photoautotrophs may have been ancient oxygen producing cyanobacteria.It can be speculated that cyanobacteria generated local and transient dioxygen oases and the need for an oxygen acceptor limited ecosystems, and they have evolved the complex biochemistry required for oxygenic photosynthesis (Sleep & Bird, 2008; see also discussion below).It can be expected that presence of O 2 influenced the redox regulated processes.
It is a widely accepted opinion that the primordial Earth's atmosphere before about 2.45 Ga was anoxic with about 10 -5 of the present atmospheric level (PAL) of molecular oxygen (Farquhar et al., 2007;Kaufman et al., 2007).The majority of geologists believe that the atmosphere started to build up significant quantities of molecular oxygen by about 2.2-2.4Ga (Cathling et al., 2001) (Fig. 1).Anoxygenic and oxygenic photosynthesis oxidized much of the Earth's crust and supplied sulphate to the ocean.Anoxygenic photosynthesis remained important until there was enough O 2 in downwelling seawater to quantitatively oxidize massive sulphides at mid-ocean ridge axes.Dioxygen remained a minuscule component of the atmosphere as long as sulphide was a significantly dissolved species in the shallow ocean (Sleep & Bird, 2008).

EvOluTION Of pHOTOSyNTHETIc ElEcTRON TRANSpORT SySTEM
Some authors suggest that the origin of photosynthesis came much later than the appearance of the last universal common ancestor (LUCA) (Fig. 1).According to this view photosynthesis arose in the Bacteria after they had separated from the Archaea (Olson & Blankenship, 2004).Molecular genetics indicates that bacteria evolved photosynthesis just once (Sadekar et al., 2006).The evolutionary histories of various classes of antenna/light-harvesting complexes reaction centers RC1 and RC2 in different organisms performing anoxygenic photosynthesis appear to be completely independent (Olson & Blankenship, 2004).The primitive photosystem might have functioned in the prebiotic phase of evolution (Olson & Blankenship, 2004).Purple bacterial RC2 and photosystem II (PSII) Fe-SODs probably constitute the most ancient group (Bannister et al., 1991).Mn-SOD certainly evolved from ancestral Fe-SOD, perhaps by way of the cambialistic SODs.Feand Mn-SODs are present both in prokaryotic and in eukaryotic organisms whereas Cu,Zn-SODs have been found mostly in Eukaryota (Alscher et al., 2002).
from oxygenic organisms have very similar overall structure and mechanisms (Olson & Blankenship, 2004).Similar arguments have been presented for the RC1 of green sulphur bacteria (later also including heliobacteria) and photosystem I (PSI) (Olson et al., 1976).The evolution of RC2 was a response to the gradual increase in the redox level of the environment as the best electron donors for CO 2 fixation were used up.The modus operandi for most bacteria containing RC2 is mainly cyclic electron flow that drives ATP production, whereas for the majority of bacteria containing RC1 it is mainly a linear electron flow that reduces ferredoxin (Olson & Blankenship, 2004) (Fig. 2).The twain Cyanobacterial photosystems evolved by the fusion of two microbes, one possesing RC1 and the other with RC2, which later developed into PSI and PSII, respectively (Xiong et al., 2000;Baymann et al., 2001;Allen & Martin, 2007).

OxygENIc pHOTOSyNTHESIS ANd REAcTIvE OxygEN SpEcIES (ROS)
The ancestral Earth's atmosphere without oxygen was not reduced, but more neutral, and probably it predominantly contained carbon dioxide (CO 2 ) (Kasting, 1993;Shaw, 2008).The emergence of oxygenic photosyntheis was a huge revolution in the young Earth environment, because a new relatively active chemical compound i.e. molecular oxygen appeared.
As photosynthesis oxygenated the environment, the formation of reactive oxygen species (ROS) would have become more common.ROS include mainly singlet oxygen ( 1 O 2 ), superoxide anion radical (O 2 -˙), H 2 O 2 , and hydroxyl radical (HO˙), all of which can cause oxidation of different molecules and in consequence disturbance of normal cellular processes leading to cell death.Therefore, in aerobic organisms an enzymatic antioxidant system against ROS has evolved in order to sufficiently detoxify ROS (Halliwell, 2006;Ślesak et al., 2007).Therefore, the co-evolution of the antioxidant system and oxygenic photosynthesis presents a paradox.Without antioxidants, oxygenic photosynthesis is self-destructive.On the other hand, without oxygenic photosynthesis, there may not have been any selective pressure for the evolution of the antioxidant system.According to the commonly accepted view, aerobic metabolism was possible only after oxygen was released into the Earth atmosphere by oxygenic photosynthesis performed by cyanobacteria, and antioxidant cellular machinery has evolved at the same time as aerobic metabolism and oxygenic photosynthesis.This statement is based on the well-known fact that ROS, mainly O 2 ˉ˙ is a toxic by-product of both respiratory and photosynthetic electron transport chains (De Las Rivas et al., 2004;Halliwell, 2006;Shaw, 2008).Two possible hypotheses concerning the sequence of events in photosynthesis-antioxidant co-evolution can be formulated; 1) if oxygenic photosynthesis evolved first, the large diffusion gradient present in the anaerobic environment would have allowed oxygen to diffuse out of the cells before being converted to ROS, no antioxidant system have been needed until the environment became more oxygenated; 2) alternatively, an antioxidant system may would have evolved first in response to abioticallyinduced ROS generation (Thomas et al., 2008).The latter hypothesis concerning earlier evolution of antioxidants should be seriously considered.Local environments on the young Earth, especially shallow oceans could be enriched in oxygen and ROS induced by UV and cosmic rays.Moreover, as was mentioned above, Borda et al., (2001) showed H 2 O 2 formation on pyrite surface in the absence of oxygen.Additionally, the widespread occurrence of basic antioxidant enzymes, such as: superoxide dismutases (SOD), superoxide reductases (SOR), catalases (CAT) and peroxidases (POD) in contemporary species from Bacteria, Archaea and Eucarya domains (Fig. 3), and even in organisms belonging to obligate anaerobes (Brioukhanov & Netrusov, 2004) might indicate that LUCA was not an obligate anaerobe.LUCA was rather a facultative anaerobe able to remove ROS if it was necessary for its own metabolism.Presence of the anti-figure 2. A simplified comparison of the photosynthetic electron transport chain in bacteria, cyanobacteria and green plants performing anoxygenic and oxygenic photosynthesis, respectively.(A) Purple bacteria do not produce oxygen, the reducing agent involved in photosynthesis in some purple sulphur bacteria is either elementar sulphur and sulphur compounds (hydrogen sulphide, sodium thiosulphate , SO 3 2-) or hydrogen and sometime simple organic compounds.The others, called purple non-sulphur bacteria, use mainly simple organic compounds (e.g.malate, succinate) although there are some bacteria that may use hydrogen and sulphur compounds (hydrogen sulphide, sodium thiosulphate) as electron donors.In these processes NAD(P)H is produced in linear electron transport as in green plants (c), this process is also observed in green bacteria (B).(B) In green filamentous bacteria (Chloroflexaceae) and green S bacteria (Chlorobiaceae) -electron are transported in a photosystem similar to PSI in green plants.Green filamentous bacteria as electron donors use hydrogen, hydrogen sulphide and some simple organic compounds; green S bacteria can use hydrogen, elementar sulphur and sulphur compounds (hydrogen sulphide, sodium thiosulphate, SO 4 2-) (adapted from Lüttge et al., 1999).
oxidant system would have protected earlier organisms performing anoxygenic photosynthesis, and supplied pre-adaptation for the subsequent evolution of oxygenic photosynthesis (Thomas et al., 2008).For this reason, most probably ancient cyanobacterial cells were already equipped with some crucial antioxidant enzymes, which they had inherited from moderately anaerobic ancestors.
One of the most important antioxidant enzymes of the first line of defence against ROS is superoxide dismutase (SOD).SOD converts superoxide anion radical (O 2 ˉ˙) to hydrogen peroxide and oxygen.Based on the metals present at the active site of an enzyme three main classes of SOD have been identified: iron (Fe-SOD), manganese (Mn-SOD) and copper/zinc (Cu/Zn-SOD) (Alscher et al., 2002).The Mn-SOD and Fe-SOD are phylogenetically related to each other and they are very similar in their primary and tertiary structures, whereas Cu/Zn-SOD shows different structural features (Fink & Scandalios, 2002;Wolfe-Simon et al., 2005).Fe-SOD has been postulated as an "archaic enzyme" (Schäfer & Kardinahl, 2003).The increasing content of oxygen in the atmosphere and the occurrence of transition metals on the young Earth might indicate that an iron form is the most "ancient" SOD (Bannister et al., 1991;Asada, 2000).In this scenario, when the early Earth atmosphere was anoxic Fe was abundant in the reduced soluble form Fe(II).For this reason it would seem that Fe(II) was the first transition metal present at the active site of the first SOD (Bannister et al., 1991).Later, during biological evolution and increasing level of O 2 in the Earth's atmosphere Fe ions were replaced by Mn, and a new SOD using Cu/Zn as metal cofactors appeared (Asada, 2000) (Fig. 1).Foyer and Allen (2003) suggest that "redox signalling" was the first type of sensory regulation that evolved in nature.Sequence similarities in higher plants to cyanobacterial redox signalling components indicate homology and suggest conserved sensory and signalling functions (Forsberg et al., 2001).Photosynthetic organisms have perfected the art of redox control.It is now widely accepted that redox signals are key regulators of plant me-tabolism, morphology, development, growth, and eventual death (Foyer & Allen, 2003).

cHlOROplASTS ARE ABlE TO cONTROl THE REdOx STATuS
Plastids are the result of cyanobacterial symbiosis which occurred over 1.2 billion years ago, the present phylogenomic data point to filamentous, heterocystforming (nitrogen-fixing) cyanobacteria as plastid ancestors (Deusch et al., 2008).There is evidence that chloroplast genome encodes proteins whose function and biogenesis are particularly tightly governed by electron transfer (Forsberg et al., 2001).Allen (2003) indicates that it may not be an accident of evolution that chloroplasts retain genes for key proteins of photosynthetic electron transport and he proposes that the reason for this retention is that the chloroplast (and also mitochondrial) genetic system enable them to respond quickly and directly to changes in their internal redox state.This response is necessary to minimise the destructive potential of free radicals (Allen & Allen, 2008).Allen and Raven (1996) suggest that the present distribution of genes among organellar and nuclear genomes is not so much a "frozen accident" but a result of selective forces favoring movement of some genes from organelles to the nucleus, due to the higher mutation frequencies of organellar genes as result of higher rates of generation of mutagenic ROS (Raven et al., 1994;Allen & Raven, 1996).

cONTROl Of REdOx STATuS IS NOT uNIfORM THROugH All pHOTOSyNTHESIzINg ORgANISMS
The redox state of the electron transport chain in chloroplasts (specifically the plastoquinone pool) is known to be responsible for post-translational modification, which allows regulation and optimisation of light harvesting in photosynthesis (Karpinski et al., 1999;Allen et al., 1981).The mechanism that couples electron transfer with gene expression is two-component redox signal transduction (Allen, 1993); the redox-controlled kinase that phosphorylates proteins in the light harvesting complex II (LHCII) and thus regulates distribution of excitation energy between the two photosystems of photosynthesis, PSI and PSII (Allen, 2003).LHCII is found in the chloroplasts of all green algae and plants (Allen, 2003).Two-component signal transduction, consisting of sensor kinases and response regulators, is the predominant signalling mechanism in bacteria.This signalling system originated in prokaryotes and has spread throughout the eukaryotic domain of life through endosymbiotic, lateral gene transfer from the bacterial ancestors and early evolutionary precursors of eukaryotic, cytoplasmic, bioenergetic organelles chloroplasts and mitochondria (Puthiyaveetil & Allen, 2009).The activity of both photosystems can be, at least partly, regulated by the number of LHCII which can migrate between them.In green algae, as much as 85 % of LHCII can migrate to PSI upon state transition (Delosme et al., 1996).The same process was also found in higher plants, although the scale of antenna relocation was much smaller about 20-30 % (Allen, 1992;Escoubas et al., 1995;Lunde et al., 2000).This migration can affect cyclic/linear ETR (electron transport rate) and thus the ATP/NADPH ratio.
Photorespiration which evolved in land plants (Asada, 2000) is a consequence of the oxygenation of ribulose-1,5-bisphosphate (RuBP) catalysed by ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO).Photorespiration not only consumes energy but it can generate metabolites, such as glycine (Madore & Grodzinski, 1984) used in metabolic pathways for the synthesis of figure 3. The universal tree of life inferred from comparative analyses of rRNA (Woese, 2000).The localization of the root of the tree of life and the nature of LUCA are still under debate.The occurrence of basic antioxidant enzymes among the three domains of life is indicated.Abbreviations: CAT, catalase; POD, peroxidase; SOD, superoxide dismutase; SOR, superoxide reductase.The key role of the redox status glutathione (Noctor et al., 1999).It is known that affinity of RubisCO to O 2 has changed during evolution which can be explained by the increasing O 2 /CO 2 ratio (Lüttge et al., 1999).Photorespiratory processes are responsible for H 2 O 2 production and increasing photorespiration also means decreasing carboxylation, both can affect the redox status of the cell (Foyer et al., 2009).In both C 4 and CAM (Crassulacean acid metabolism) representing about 10 % of all plants are able to concentrate CO 2 around RubisCO to avoid strong photorespiration, however, in CAM plants this is true only when a sufficient amount of bicarboxylic acids is available (Miszalski et al., 1998).Some plant families such as Clusiaceae and Aizoaceae are extremely flexible and can switch between C 3 and CAM, and this was shown to be parallel to changes in redox status (Miszalski et al., 2001;Lüttge, 2007;Kornas et al., 2009;2010).
Excess energy excitation (EEE) which cannot be converted into chemical energy can also be dissipated by electron transport to O 2 in the Mehler-peroxidase, waterwater cycle pathway or as heat by non-photochemical quenching.Non-photochemical quenching is linked to the formation of zeaxanthin in the xanthophyll cycle and an increased proton gradient across the thylakoid membrane (Ruban & Horton, 1995).The light-dependent xanthophyll conversion is essential for the adaptation of algae and plants to different light conditions and allows a reversible switch of photosynthetic light-harvesting complexes between a light-harvesting state under low light and a dissipative state under high light (Jahns et al., 2009).Three different xanthophyll cycles have been described in the literature: the violaxanthin cycle (Vxcycle; in all plants and green algae) (Siefermann-Harms, 1985), the diadinoxanthin cycle (Ddx-cycle; in some algae) (Stransky & Hager, 1970) and the lutein-epoxide cycle (Lx-cycle; found in some plant species) (Bungard et al., 1999;García-Plazaola et al., 2007).Xanthophyll cycle regulation is partly under the control of O 2 produced in the water splitting system in chloroplasts.Possibly, this could happen at a relatively low atmospheric concentration of O 2 .
Chloroplasts of algae and higher plants originate from a cyanobacterial endosymbiont, which was originally competent for both photosynthesis and respiration (Jans et al., 2008).Chloroplasts have not entirely lost competence for oxidizing NAD(P)H at the expense of oxygen.In chlororespiration, a thylakoid electron transport pathway involving NAD(P)H:plastoquinone oxidoreductase and plastoquinol oxidase activities takes place (Peltier & Cournac, 2002).Genes encoding several subunits of a NAD(P)H-dehydrogenase (Ndh) involved in a chlororespiration complex homologous to mitochondrial complex I were found in the chloroplast genome of higher plants (Shimada & Ugiura, 1991).In the plastoquinol (PQH 2 )oxidizing part of the chlororespiratory pathway an alternative plastid terminal oxidase (PTOX) is present which shows homology to the mitochondrial alternative oxidase (AOX) (Carol et al., 1999).This plastid terminal oxidase (PTOX) was also detected in green microalgae in which it was suggested to function as an overflow device for excess PQH2 (Jans et al., 2008).The structure of the Ndh complex has remained obscure, and therefore the role of several Ndh-associated nuclear-encoded proteins either as auxiliary proteins or as structural subunits remains uncertain (Suorsa et al., 2009).
PSII is characterized by its vulnerability to light, which induces its inactivation and subsequent damage and degradation of the D1 reaction center protein.
Many experimental studies have focused on the light-dependent translation of psbA mRNA, which encodes the D1 protein.In the unicellular algae (Chlamydomonas reinhardtii) translation initiation of D1 may be mediated by the chloroplast redox state and ADP-dependent phosphorylation induced by light (Kim & Mayfield, 1997).In higher plants translation of D1 is also strictly light regulated (Mühlbauer & Eichacker, 1998).

HOW dO plANTS AdApT TO flucTuATINg ENvIRONMENTAl cONdITIONS?
One of the major ways in which plants transmit information about the changing environmental factors is the ROS sensing, producing and scavenging system.Abiotic and biotic stressors regardless of the first target site of their action, affect the cellular balance between different redox buffers and oxidants, called redox homeostasis (Mahalingam & Fedoroff, 2003;Apel & Hirt, 2004;Dizengremel et al., 2009).A lot of evidence points to this phenomenon as a common background of most, if not all, environmental stresses perceived not only as a source of oxidative stress, but also as a mechanism controlling the main aspects of plant adaptation to various growth conditions (Foyer & Noctor, 2005a;2009).The interplay between ROS production and scavenging determines the steady-state level of ROS in cells, as well as the ROS signature, i.e. the duration, localization, and amplitude of ROS signals conditioning stress responses (Mahalingham & Fedoroff, 2003;Miller et al., 2008).
Many studies have established that ROS and antioxidants could function as intracellular messengers under stress as well as under normal growth conditions.ROS produced by plasma membrane-bound NADPH oxidase have recently been shown to play a role not only in the well-recognized defence responses against biotic stress (Wojtaszek, 1997;Shetty et al., 2008) but also during plant signalling and development (revieved by Laloi et al., 2004).Evidence has been provided that NADPH oxidase produces ROS that activate Ca 2+ channels responsible for the formation of the tip-high Ca 2+ gradient required for the elongation of root hairs (Foreman et al., 2003).Moreover, ROS, and especially H 2 O 2 , produced by NADPH oxidases have been shown to act as key regulators in physiological processes such as stomatal closure and seed germination known to be under the control of abscisic acid, and root gravitropism controlled by auxins (Apel & Hirt, 2004;Laloi et al., 2004).This crosstalk of ROS with Ca 2+ -and hormone-signalling might provide a link to downstream signalling pathways implicated in a wide range of growth and developmental processes.ROS are also involved in regulation of programmed cell death (PCD) in plants, a phenomenon essential for plant growth, development and adaptation to the fluctuating environmental conditions (Foyer & Noctor, 2005b).ROS-controlled PCD occurs during the aleurone cell death in germinating seeds of monocots and leaf senescence.The increase in cellular ROS concentration is a prerequisite for induction of the hypersensitive response (HR), one of the best reviewed examples of plant PCD (Levine et al., 1994;Jabs, 1999;Kuźniak et al., 2010).HR is genetically controlled and involves activation of plant host defence-related genes and various defence responses (Lamb & Dixon, 1997;Suh et al., 2003).
Recent genetic evidence suggests that ROS do not trigger PCD or senescence by causing damage to the cell but they act as signals that activate pathways of gene expression that lead to genetically regulated cell death (Foyer & Noctor, 2005a;Dietz, 2008).However, the biological activity of ROS in all these developmental and stress processes needs to be viewed in connection with other reactive molecules, especially nitric oxide (NO), that affect both the accumulation and function of ROS (Wilson et al., 2008).It is apparent that the effect of ROS/NO interplay depends on their concentrations and the status of the environment (Hayat et al., 2010).
Most environmental conditions that impose constraints on plant growth and development promote an increase in excess excitation energy (EEE) thus influencing light energy capture and carbon fixation by photosynthesis that are the key determinants for plant life.Stresses affect the photosynthetic electron transport and change the efficiency of light energy fixation (Bechtold et al., 2005;Zhou et al., 2007).Under these stressful conditions imbalance between light energy absorbed through PSII and the ultimate consumption of the photosynthetic electrons through metabolic pathways such as the Calvin cycle, photorespiration and nutrient assimilation occurs.This leads to an increased formation of ROS and to photooxidative stress.For example, drought-, salinity-or low temperature-induced stomatal closure inhibits CO 2 assimilation and NADP + regeneration by the Calvin cycle while at the same time the light-driven photosynthetic electron transfer proceeds at high rates leading to an overreduction of the electron transport chain.Consequently, the formation of ROS is initiated at the PSI site by the transfer of electrons to alternative acceptors, predominantly molecular oxygen.Similarly, excitation pressure may be induced by the lack of essential nutrients because of limitations in the availability of electron acceptors such as NO 3 -or SO 4 2- (Wilson et al., 2006).Thus, the photosynthetic apparatus of organisms as diverse as algae, cyanobacteria and higher plants has emerged as a global redox sensor which detects and processes the incoming environmental signals (Huner et al., 1998).Messages originating from chloroplasts influence the expression of defence and regulatory genes thus modulating either the acclimatory process or the execution of PCD.
Three classes of redox signals originating from chloroplasts can be considered to be important in governing the plant adaptive/stress response in natural environments (Pfannschmidt et al., 2001).Class 1 originates from specific redox pairs in the photosynthetic electron transport (PET) chain e.g. the reduced and oxidized plastoquinone and the cytochrome b 6 f complex.Class 2 depends on the redox state of stromal thioredoxin, NAD(P)H, glutathione and ascorbate whereas class 3 is mediated by ROS.These signals act in chloroplasts to ensure the most effective operation of photosynthesis.The redox state of the plastoquinone pool feeds into this mechanism and chloroplast sensor kinase is proposed to monitor the electron transport coupling the redox state of plastoquinone to gene expression in chloroplasts.It passes the information of the electron flux in the PET chain to response regulatory proteins that switch the photosystem genes on and off (Puthiyaveetil & Allen, 2009).Moreover, redox signals of chloroplast origin reach other compartments and coordinate photosynthesis with other cellular activities exerting a multilevel control on the regulation of gene expression in the nucleus (retrograde signalling) and metabolic activities in mitochondria and cytoplasm (Oelze et al., 2008) (Fig. 4).Retrograde signalling regulates the expression of nuclear organelle genes in response to the metabolic and developmental state of the organelle (Pfannschmidt et al., 2009).Besides the cross-talk between chloroplasts/ mitochondria and the nucleus (Fey et al., 2005;Rhoads & Subbaiah, 2007), chloroplast-mitochondrion redox communication has been established during plant evolution to coordinate the activities of these two bioenergetic organelles to enable an optimized acclimation response Connections between chloroplasts and other cellular compartments are indicated.Abbreviations: ASC, reduced ascorbate; DHA, oxidized ascorbate; Grx, glutaredoxin; GSH, reduced glutathione; GSSG, oxidized glutathione; MET, mitochondrial electron transport; PET, photosynthetic electron transport; ROS, reactive oxygen species; Trx, thioredoxin.The key role of the redox status (Leister, 2005).For example, the mitochondrial alternative oxidase is involved in the removal of excess photosynthetic reducing power via the malate valve.Excess reducing power can be shuttled out of plastids in the form of malate and the reducing equivalents released by the action of mitochondrial NADH/NAD + -dependent malate dehydrogenase converting malate to oxaloacetate are consumed by an alternative oxidase preventing the chloroplast from overreduction under unfavourable conditions such as drought and excess light (Scheibe, 2004).Besides malate other products of photosynthetic activity such as glycine or NAD(P)H can also contribute to mitochondrial respiration balancing the cellular energy and redox status (van Lis & Atteia, 2004).Part of this regulatory mechanism centres around ROS, which are unavoidable by-products of photosynthesis, namely H 2 O 2 and 1 O 2 generated at PSI and PSII, respectively, that have been associated with the control of nuclear gene expression (Op den Camp et al., 2003;Pfannschmidt et al., 2009).Moreover, photorespiratory H 2 O 2 has been proposed to have an impact on the transcription of nuclear genes (Vandenabeele et al., 2004).
One of the best characterized mechanisms of redox signalling in photosynthetic organisms is that mediated by dithiol/disulphide exchanges under the control of thioredoxins (TRXs).The redox proteomic approach revealed that in Arabidopsis all 11 enzymes of the Calvin cycle can be regulated by TRXs (Meyer et al., 2005).At present, however, the redox-dependent thiol/disulphide transition extends beyond the well characterized TRXmediated regulation of the Calvin cycle enzymes (Lemaire et al., 2007) and is considered to be one of the most important modifications affecting many cell protein functions (Buchanan & Balmer, 2005).TRXs are implicated in different aspects of plant life including development and adaptation to environmental changes and stresses (Meyer et al., 2008).Because H 2 O 2 is a mild oxidant that can oxidize thiol groups, it has been speculated that H 2 O 2 generated under stress could also be sensed via modification of thiol residues in target proteins (Pitzschke et al., 2006).
The molecular responses to oxidative stress are regulated by redox-sensitive transcription factors.To date, the activation of NPR1 protein (Nonexpressor of Pathogenesis-Related protein 1) is one of the best-known examples.NPR1 was identified as a redox-sensitive transcription factor in Arabidopsis.The reduction of NPR1 preceding gene induction requires an increase in reduced glutathione content and a concomitant shift in the cellular redox environment toward reducing conditions (Mou et al., 2003;Fobert & Despres, 2005).Under these conditions, NPR1 is reduced from an inactive oligomeric complex localized in the cytosol to an active monomeric state through the reduction of intermolecular disulphide bonds.Monomeric NPR1 is then translocated into the nucleus where it interacts with transcription factors of the TGA class (Mou et al., 2003;Pieterse & Van Loon, 2004).

cONcluSIONS
Most studies on the redox status of the cell were performed on higher plants and algae.We show that antioxidant defences have a long history.Plants can control the cell's redox status using a wide spectrum of different mechanisms and this status is used to control nearly every aspect of plant biology from chemistry to development, growth, and eventual death (Foyer & Allen, 2003).
All aspects of aerobic life involve ROS, RNS, antioxidants and redox regulation.In recent years our knowledge about the role of oxidative stress and redox regulation of cell functions has increased remarkably with the result that the classical definition of the oxidative stress proposed by Sies in 1985 and describing it as a disturbance in the prooxidant-antioxidant balance in favour of the former, leading to potential damage has been replaced by that of Jones in 2006.This new definition emphasizes the significance of redox regulations and describes oxidative stress as a disruption of redox signalling and control.Various redox-active compounds are involved in these processes, including pyridine nucleotides, thioredoxins, glutaredoxins and other thiol/disulphide-containing proteins.These redox regulations, integrated with the redox-reactions in photosynthesis and respiration to achieve an overall energy balance and to maintain a reduced state necessary for the biosynthetic pathways that are reductive in nature.It underlies the physiological and developmental plasticity in plant response to the environmental signals.

figure 4 .
figure 4. Schematic representation of general pathways of redox regulation that control gene expression and enzyme activity in response to environment-induced changes in photosynthesis (adapted from van lis & Atteia, 2004).Connections between chloroplasts and other cellular compartments are indicated.Abbreviations: ASC, reduced ascorbate; DHA, oxidized ascorbate; Grx, glutaredoxin; GSH, reduced glutathione; GSSG, oxidized glutathione; MET, mitochondrial electron transport; PET, photosynthetic electron transport; ROS, reactive oxygen species; Trx, thioredoxin.