REVIEW ARTICLE published: 27 December 2012 doi: 10.3389/fpls.2012.00292 ROS-talk – how the apoplast, the chloroplast, and the nucleus get the message through

Alexey Shapiguzov, Julia P. Vainonen, Michael Wrzaczek and Jaakko Kangasjärvi* Division of Plant Biology, Department of Biosciences, University of Helsinki, Helsinki, Finland

Edited by: The production of reactive oxygen species (ROS) in different plant subcellular compart- Dario Leister, Ludwig Maximilian ments is the hallmark of the response to many stress stimuli and developmental cues. University of Munich, Germany The past two decades have seen a transition from regarding ROS as exclusively cytotoxic Reviewed by: agents to being considered as reactive compounds which participate in elaborate signaling Daniel Hofius, Swedish University of Agricultural Sciences, Sweden networks connecting various aspects of plant life. We have now arrived at a stage where it Markus Wirtz, Centre for Organismal has become increasingly difficult to disregard the communication between different types Studies, Germany and pools of ROS. Production of ROS in the extracellular space, the apoplast, can influ- Veronica G. Maurino, Heinrich-Heine- University Düsseldorf, Germany ence their generation in the chloroplast and both can regulate nuclear gene expression. In spite of existing information on these signaling events, we can still barely grasp the *Correspondence: Jaakko Kangasjärvi, Division of Plant mechanisms of ROS signaling and communication between the organelles. In this review, Biology, Department of Biosciences, we summarize evidence that supports the mutual influence of extracellular and chloroplas- University of Helsinki, Viikinkaari 1, tic ROS production on nuclear gene regulation and how this interaction might occur. We P.O. Box 65, FIN-00014 Helsinki, Finland. also reflect on how, and via which routes signals might reach the nucleus where they are e-mail: jaakko.kangasjarvi@helsinki.fi ultimately integrated for transcriptional reprogramming. New ideas and approaches will be needed in the future to address the pressing questions of how ROS as signaling molecules can participate in the coordination of stress adaptation and development and how they are involved in the chatter of the organelles.

Keywords: ROS signaling, apoplast, chloroplasts, retrograde signaling, Arabidopsis thaliana

INTRODUCTION signal. ROS are generated in many compartments of plant cells. During their life plants face a vast set of environmental chal- Whereas the “ROS landscape” of the animal cell is dominated by lenges: extreme changes in ambient illumination, temperature, mitochondria as the main source of ROS (Marchi et al., 2012), the and humidity, differences in soil salinity, attack by pathogens and role of these organelles in ROS production in plants is more sub- herbivores, mechanical wounding, etc. Towithstand all these chal- tle (Dutilleul et al., 2003; Suzuki et al., 2012) and is not addressed lenges, plants have developed a repertoire of signaling pathways in this review. Apart from mitochondria, ROS are produced in that is unparalleled in its complexity among living organisms. Sig- the chloroplasts, the peroxisomes, and the apoplast, as well as in naling through plant hormones (Vanstraelen and Benková, 2012), less commonly known locations, the nucleus and the endoplasmic cell surface receptors (Geldner and Robatzek, 2008), and light reticulum (Overmyer et al., 2003; Ashtamker et al., 2007; Foyer and perception by plastids and photoreceptors (Kami et al., 2010)are Noctor, 2009; Jaspers and Kangasjärvi, 2010; Mazars et al., 2010). integrated in the cell to eventually reprogram gene expression and Yet uncharacterized signaling networks between the organelles that metabolism and shape strategic decisions on plant stress response employ ROS as second messengers have recently raised consider- and development (Jaillais and Chory, 2010). able interest (Figure 1). For example, ROS that are produced in A critical role in this signal integration and decision-making the chloroplast have been implicated as intermediates in retrograde is played by a class of reactive forms of the molecular oxygen, signaling from chloroplast to nucleus during acclimation of pho- collectively referred to as reactive oxygen species (ROS; Murphy tosynthesis (Nott et al., 2006; Galvez-Valdivieso and Mullineaux, et al., 2011; Kangasjärvi et al., 2012). ROS, including singlet oxy- 2010). Intriguingly, however, it has recently been realized that the 1 •− gen ( O2), superoxide (O2 ), hydrogen peroxide (H2O2), and role of this signaling goes beyond optimization of photosynthesis: hydroxyl radical (•OH) are unavoidable by-products of aerobic chloroplastic ROS production and photosynthetic functions are metabolism (Imlay, 2003, 2008; Ogilby, 2010)whichhavetradi- also regulated by cues that are perceived in the cell wall, frequently tionally been regarded mainly as damaging cytotoxic agents. In referred to as the extracellular space or the apoplast (Padmanab- line with this view, life has developed a plethora of ROS scav- han and Dinesh-Kumar, 2010). Thus, the sensu stricto retrograde enging systems including the low-molecular weight compounds signaling (from chloroplast to nucleus) can also be regarded as a ascorbic acid and glutathione (Foyer and Noctor, 2011)aswell part of a larger network where apoplastic signals induce the gener- as different classes of antioxidant enzymes (Apel and Hirt, 2004). ation of ROS in the chloroplast, which in turn leads to regulation During the recent years, however, a new concept has emerged of nuclear gene expression by several still uncharacterized, but where ROS play important signaling roles during development at least partially chloroplast-derived, ROS-dependent retrograde and stress responses, and controlled production of ROS acts as a signals.

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Abiotic stress Biotic stress Systemic signaling Apoplast ROS Local signaling

Nucleus ROS

Chloroplast

FIGURE 1 | Reactive oxygen species (ROS)-talk in plant cells. Biotic and networks. Apoplastic ROS signaling can also reach the nucleus through abiotic stimuli lead to the generation of ROS in the apoplast which is cytosolic pathways directly. Yellow arrows demonstrate intracellular subsequently communicated to the inside of the cell where the signal leads transmission of apoplastic and chloroplastic ROS-induced signals where they to an increase in chloroplastic ROS production. The chloroplast can further connect neighboring cells (local signaling) or participate in long-distance amplify the signal and transmit it to the nucleus via various cytosolic signaling (“systemic”) signaling throughout the plant (red arrows).

ROS IN THE APOPLAST by plant cells remains unclear. It is not known how the signal Likely candidates involved in the apoplast-to-chloroplast signal- is transmitted to the cytoplasm, the chloroplasts and eventually ing are ROS produced in the cell wall. Their accumulation in the nucleus and what are the interactions between the differ- •− response to different abiotic and biotic stimuli during the so- ent subcellular compartments. The possibility of O2 itself being called apoplastic “oxidative burst” depends on several classes of the mediator of downstream signaling would require superoxide- enzymes, including cell wall peroxidases (Bindschedler et al.,2006) specific extracellular receptors or anion channels in the direct •− and plasma membrane NADPH oxidases (Figure 2; Torres et al., vicinity to the site of O2 production (Browning et al., 2012). 2002; Suzuki et al., 2011). The latter enzymes, commonly known Anion channels have been shown to mediate superoxide import as respiratory burst oxidase homologs (Rboh) are transmembrane in mammalian cells (Hawkins et al., 2007) thereby linking extra- flavoproteins that oxidize cytoplasmic NADPH, translocate elec- cellular and intracellular ROS signaling. Analogous systems in trons across plasma membrane and reduce extracellular ambient plants have so far not been identified. Unlike superoxide, the •− ∼ (triplet) oxygen to yield O2 in the cell wall. Due to its charge, this H2O2 molecule is relatively stable (with a half-life of 1 ms) short-lived ROS is unable to passively cross the lipid bilayer and under physiological conditions and in many respects resem- remains in the apoplast, where it is rapidly converted into another bles a molecule of water. Its dipole moment, similar to that of species, H2O2, either spontaneously or in a reaction catalyzed by H2O, limits passive diffusion of H2O2 through biological mem- the superoxide dismutase (SOD; Browning et al., 2012). The func- branes. Possible candidates for the import of apoplastic H2O2 tions of plant NADPH oxidases stretch beyond stress responses are aquaporins (Figure 2), a ubiquitous family of channel pro- and include roles in development (Sagi and Fluhr, 2006; Takeda teins that has undergone an extensive expansion in vascular plants et al., 2008), in sodium transport in the xylem sap (Jiang et al., (Zardoya, 2005; Soto et al., 2012). Recent studies have identified 2012), and intriguingly also in long-distance (“systemic”) ROS sig- several aquaporins as specific H2O2 transporters in Arabidopsis naling (Miller et al., 2009). In Arabidopsis wounding, heat stress, (Bienert et al., 2007; Dynowski et al., 2008; Hooijmaijers et al., high light, and increased salinity result in RbohD-dependent sys- 2012). However, further research is required to assess the role temic spread of the oxidative burst along the rosette leaves. The of H2O2 transport during the oxidative burst. In addition to 2+ •− signal is triggered by intracellular Ca spiking at the wounding transport across membranes, O2 and H2O2 maybesensedby site. It is propelled by accumulation of ROS in the apoplast and a number of apoplastic compounds. Oxidation of extracellu- by – still unidentified – symplastic signals, one of which might lar pools of glutathione and ascorbic acid might play a role in be ROS production in chloroplasts: results by Joo et al. (2005) transmitting the redox signal to the cytosol (Destro et al., 2011; suggest that chloroplastic ROS is required for intercellular ROS Foyer and Noctor, 2011; Noctor et al., 2012). ROS can also be signaling. This ROS “wave” travels across an Arabidopsis rosette perceived by the apoplastic proteins and/or plasma membrane- at a rate of approximately 8 cm per minute (Miller et al., 2009). localized receptors through redox modification of their cysteine Taken together, the currently available data suggests different roles residues (Figure 2). Those putative receptors or other sensory sys- for ROS in strictly localized signaling events but also in systemic tems for extracellular ROS in plants have so far remained elusive, signaling. but for example, several classes of receptor-like protein kinases We have obtained a good understanding of the processes in (RLKs) with cysteine-rich extracellular domains (most notably which apoplastic ROS are involved, but how they are perceived the CYSTEINE-RICH RLKs, CRKs) have been suggested to be

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- Peroxidases HO22 O 2 Ca2+ AP ? ? O AQP 2 Rboh

RLK ? ? Ca2+ ? MAPK ? HO22 CAS SA 1 O 2

EX1 Transcriptional EX2 ETC

response - O 2

HO22 AQP? ?

1 FIGURE 2 | Reactive oxygen species (ROS) signaling networks electron transfer chain (ETC) subsequently increases. Singlet oxygen ( O2) •− connecting apoplast, chloroplast and nucleus. Apoplastic ROS are and O2 /H2O2 are produced in different domains of ETC. Elevated ROS produced by extracellular peroxidases (hydrogen peroxide; H2O2) and plasma inside the chloroplast results in transcriptional reprogramming through •− membrane-bound NADPH oxidases, Rboh. Superoxide (O2 ) is then identified (e.g., EXECUTER1/2, EX1/EX2, rupture of chloroplast envelope) and •− unknown components of the retrograde signaling but also through hormone converted to H2O2.H2O2 (and possibly O2 ) might enter the cell through plasma membrane channels (aquaporins, AQP) and/or react with extracellular signaling, e.g., increased production of the stress hormone salicylic acid (SA). (apoplastic protein, AP) or transmembrane sensor proteins (e.g., receptor-like Channel proteins (AQP) might also allow ROS leak from the chloroplast to the 2+ kinases, RLKs) ultimately resulting in changes in gene expression through cytoplasm. Calcium (Ca ) is involved in the regulation of ROS production in intracellular signaling pathways, involving, for example, MAPKs the apoplast and the chloroplast. In the latter case it acts through the sensory (mitogen-activated protein kinases). Extracellular ROS production is sensed protein CALCIUM-SENSING RECEPTOR (CAS) but the mechanisms are still via yet unknown mechanisms in the chloroplast where ROS generation by the unclear. involved in ROS perception (Shiu and Bleecker, 2003; Wrzaczek response is evident in various model systems and processes (Joo et al., 2010). et al., 2005; Vahisalu et al., 2010), although it is mechanistically still largely unexplained. The results suggest that the apoplastic FROM BEYOND TO HERE, SIGNALS FROM THE ROS signal is transduced to the chloroplasts, where a secondary EXTRACELLULAR SPACE ROS production is initiated. This signal transmission might use What happens in the plant cell after an extracellular oxidative burst cytosolic signaling components. Also, the location of chloroplasts has been triggered? A connection of apoplastic and chloroplas- close to the plasma membrane might facilitate direct communica- tic ROS into common signaling networks during the plant stress tion between the two organelles. Thus, the chloroplast can act as

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an “amplifier,” or “execute” the signal received from the apoplast in the photosynthesizing plant tissues chloroplasts are able to pro- (Figure 1). duce the most massive pools of ROS among different subcellular One of the examples of such a role of chloroplasts is the plant compartments. immune response to pathogens that is accompanied by a bi-phasic Generation of ROS in the chloroplasts depends on multiple accumulation of ROS. The first phase occurs within tens of min- aspects of chloroplast physiology including photosynthesis, gene utes from the onset of infection. It is mostly apoplastic and is expression, chlorophyll (tetrapyrrole) biosynthesis, and hormonal tightly linked to NADPH oxidase activity (Figure 2). The sec- control (Asada, 2006; Sierla et al., 2012). For example, the pro- •− ond increase in ROS production happens several hours after the duction of O2 /H2O2 by photosystem I (PS I) varies according pathogen attack (Lamb and Dixon, 1997; Jones and Dangl, 2006). to changing photosynthetic electron transfer and CO2 fixation During this stage of response the infected cells might undergo pro- rate. Extracellular stimuli, such as recognition of bacterial com- grammed cell death (PCD) leading to the collapse of the infected ponents by the plasma membrane receptors, can rapidly regulate tissue and, in the case of biotrophic pathogens, to suppression chloroplastic functions. During plant–pathogen interactions the of pathogen growth. This specialized form of pathogen-triggered cues perceived in the apoplast trigger MAPK cascades (Figure 2) PCD is a part of the hypersensitive response (HR). Different and result in fast down-regulation of photosynthetic genes and subcellular compartments including apoplast, chloroplasts, mito- accumulation of H2O2 in chloroplasts that is necessary for initia- chondria, and peroxisomes contribute to ROS production during tion of HR-mediated cell death (Liu et al., 2007). Another example HR, but a growing amount of evidence suggests a crucial role is the transient decrease in the ability of PS II to dissipate exces- for the chloroplast in this process (Yao and Greenberg, 2006; sive light energy as heat via non-photochemical quenching (NPQ) Liu et al., 2007; Zurbriggen et al., 2009, 2010). Silencing of the at an early stage of pathogen recognition. This decrease in NPQ chloroplast redox proteins peroxiredoxin and NADPH-dependent makes chloroplasts more predisposed to the production of ROS, thioredoxin reductase C that scavenge chloroplastic H2O2 led to which might be a priming mechanism for chloroplast ROS sig- spreading PCD in response to application of coronatine, a phy- naling at later stages of immune response (Göhre et al., 2012). totoxin with structural similarity to jasmonic acid produced by Several chloroplastic redox hubs, including the plastoquinone as several pathogenic strains of Pseudomonas (Ishiga et al., 2012). well as the glutathione pools and the thioredoxin system, pro- The involvement of chloroplasts in plant immunity is further sup- vide not only dynamic local regulation of photosynthesis, but also ported by the observation that the pathogen resistance of plants might communicate the chloroplast redox status to the cytosol differs between light and dark (Roden and Ingle, 2009) and by (Marty et al., 2009; Bashandy et al., 2010; Foyer and Noctor, 2011; the fact that several bacterial and viral elicitors interact with Noctor et al., 2012; Rochaix, 2012). For example, the redox state chloroplast-targeted proteins or are imported into chloroplasts of plastoquinone, a component of photosynthetic electron trans- (Padmanabhan and Dinesh-Kumar, 2010). Thus, not only the fer chain, is monitored through the thylakoid-associated protein apoplast and the cytosol, but also the chloroplasts are strategic kinase STATE TRANSITION 7 (STN7). STN7-dependent phos- battlefields during the defense against pathogens (Padmanabhan phorylation of chloroplast proteins leads on the one hand to and Dinesh-Kumar, 2010). optimization of photosynthesis in response to changing light con- Chloroplast-generated ROS are not only involved in initiat- ditions (via the reversible reallocation of light-harvesting antennae ing and promoting cell death during the HR, but also in the called state transitions) and on the other hand to a retrograde up-regulation of defense-related genes, down-regulation of pho- signal (Bonardi et al., 2005; Rochaix, 2012). Another chloroplast tosynthesis genes and even in limiting the spread of the cell death protein kinase, CHLOROPLAST SENSOR KINASE (CSK), cou- (Straus et al., 2010). For example, a significant portion of the ples plastoquinone redox state to the regulation of chloroplast gene genes induced by artificial metabolic overproduction of H2O2 via expression (Puthiyaveetil et al., 2012). The soldat8 mutation in the expression of glyoxylate oxidase in the chloroplasts (Balazadeh chloroplastic RNA polymerase SIGMA SUBUNIT 6 (SIG6)gene 1 et al., 2012), are also induced by chitin, a well-known elicitor of increases the tolerance of seedlings to O2 (Coll et al., 2009), which the apoplastic oxidative burst and downstream pathogen defense links chloroplast transcriptional control to the ROS signaling. The responses. Similarly, silencing of thylakoid ascorbate peroxidase RNA-binding chloroplast protein GENOMES UNCOUPLED 1 (tAPX) led to an increase in H2O2 production and to activation (GUN1) is implicated both in chloroplast translation and tetrapyr- of defense responses (Maruta et al., 2012), including the accumu- role biosynthesis and is somehow involved in retrograde signaling lation of the stress hormone salicylic acid (SA), a central mediator (Czarnecki et al., 2011; Woodson et al., 2012). GUN1, and one of of plant pathogen defense. These examples underline that H2O2 the key components of tetrapyrrole biosynthesis, the ChlH sub- accumulation in the chloroplast and the related retrograde signal- unit of magnesium chelatase, are also involved in abscisic acid ing are involved in the activation of defense genes during responses signaling (Shen et al., 2006; Koussevitzky et al., 2007; Cutler et al., to pathogens. 2010; Shang et al., 2010). The heme, the product of a side branch of tetrapyrrole biosynthesis, exits chloroplasts to be used as a CHLOROPLASTS AS THE PET PEEVE OF THE PLANT CELL cofactor by numerous hemoproteins in the cell and to provide Why does the plant cell involve the chloroplast, the major site positive feedback on transcription of nuclear genes that encode of energy production and biosynthesis in stress responses? One chlorophyll-binding proteins of chloroplasts (Nott et al., 2006; explanation is that photosynthesizing chloroplasts continuously Woodson et al., 2011, 2012; Czarnecki and Grimm, 2012). The dis- produce ROS due to numerous electron transfer reactions in the turbance of the cell affects the delicate physiological equilibrium presence of oxygen (Foyer and Noctor, 2003; Asada, 2006). Hence, of the chloroplasts resulting in elevated ROS production.

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CHLOROPLASTIC ROS AS SIGNALS phosphorylated by the thylakoid protein kinase STN8 (Vainonen Plant cells have over the course of evolution learned to use et al., 2008), a paralog of STN7, which suggests a link between chloroplastic ROS for signaling purposes. Several studies have the CAS activity and the redox state of the plastoquinone pool. demonstrated a central role for the highly reactive singlet oxy- However, CAS is not only involved in light-dependent retrograde 1 gen ( O2) as a chloroplastic signal involved in the regulation of signaling: also various abiotic or biotic stress stimuli activate CAS plant cell death. PS II and its light-harvesting antennae produce through a yet unknown mechanism. This activation leads to real- 1 2+ O2 when light-excited chlorophylls adopt the rare triplet state and location of Ca ions within the chloroplast and to accumulation 1 then reduce triplet oxygen (Krieger-Liszkay et al., 2008). Produc- of O2, which, in turn, initiates defense responses through an 1 tion of O2 is enhanced when the light-excited electrons cannot unidentified retrograde signal (Nomura et al., 2012). Thus, CAS 1 escape PS II chlorophylls because the downstream components appears to act in the O2-dependent retrograde signaling pathway of electron transfer chain (mainly the plastoquinone pool) are discussed above. already over-reduced, a situation typical of excessive illumination. Another source of ROS in chloroplasts is PS I. Its electron- 1 •− O2 readily reacts with lipids, proteins, and pigments and is rapidly donor side generates O2 that is scavenged by chloroplast SOD quenched by water, which makes its diffusion distance from the to form H2O2 (Asada, 2006). H2O2, in turn, is reduced to water site of production shortest among all ROS (Asada, 2006). For that by a number of enzymes including ascorbate peroxidase (APX), 1 reason O2 is unlikely to leave the chloroplasts, but several prod- peroxiredoxin, and glutathione peroxidase. H2O2 produced in 1 ucts of O2-dependent lipid or carotenoid oxidation, including chloroplasts gives rise to retrograde signals. The signaling is not oxylipins (op den Camp et al., 2003; Przybyla et al., 2008) and well understood and might be a combination of passive diffusion volatile β-cyclocitral (Ramel et al., 2012), are suspected to act as of H2O2with indirect pathways including hormonal (abscisic acid) 1 the O2-dependent retrograde signal. signaling (Mullineaux and Karpinski, 2002; Galvez-Valdivieso and The Arabidopsis flu mutant (Meskauskiene et al., 2001) has Mullineaux, 2010). The possibility of H2O2 leakage from chloro- 1 beenusedasagenetictooltoidentify O2-responsive genes and to plasts is supported by the fact that a knockout of cytosolic APX1 1 dissect signaling pathways triggered by O2 production in chloro- leads to hypersensitivity of the photosynthetic apparatus to light plasts. The chloroplast-localized FLU protein inhibits one of the stress (Davletova et al., 2005). Diffusion of H2O2 from chloro- early enzymes of tetrapyrrole biosynthesis. Flu seedlings are unable plasts has also been demonstrated in vitro (Mubarakshina et al., to control the biosynthetic pathway through negative feedback and 2010). Aquaporins in the chloroplast envelope (Figure 2)seemto accumulate the chlorophyll precursor protochlorophyllide in the be involved in this H2O2 leakage (Borisova et al., 2012), but how dark. Being transferred to light, the seedlings bleach and die due to the aquaporins are regulated is unknown. In any case, H2O2 itself 1 the massive generation of O2 in their chloroplasts. This death is is not likely to be the retrograde signaling substance that directly primarily caused by a profound reprogramming of nuclear tran- affects nuclear gene expression. More probably, it is sensed by 1 scription rather than by mere chemical toxicity of O2 (op den compartment-specific redox-sensitive components, which medi- Camp et al., 2003). In addition, shortly after the exposure of flu ate the signal to the nucleus (Sierla et al., 2012). Oxidized proteins seedlings to light, their chloroplasts rupture releasing the soluble or peptides have been suggested as one of the possible downstream stroma into the cytosol – this resembles the leakage of mitochon- mediators of such H2O2 signaling (Wrzaczek et al., 2009; Møller drial proteins to the cytosol during the mitochondria-triggered and Sweetlove, 2010). PCD. Two homologous chloroplast proteins EXECUTER1 and EXECUTER2 (Figure 2) conserved in higher plants are involved in THE FRUSTRATING COMPLEXITY OF ROS RESPONSES this process, although their exact role is unknown (Wagner et al., One of the most frequently employed tools to investigate the role •− 2004; Lee et al., 2007; Kim et al., 2012). It should be noted that of O2 in the chloroplast is the herbicide methyl viologen (MV; 1 •− although O2-dependent PCD is significantly exacerbated in flu,it also known as paraquat). MV accelerates the production of O2 is not confined to the mutant but is also observed in wild-type Ara- by PS I and inhibits APX, leading to the accumulation of H2O2 in bidopsis under severe light stress (Kim et al., 2012). The sensory MV-treated plants (Mano et al., 2001). Comparison of the tran- 1 and signaling systems involved in the transmission of the chloro- scriptional responses to O2 and H2O2 using the flu mutant and 1 plastic O2-dependent signal to nucleus have not been identified, the plants treated with MV demonstrated the specific and to a large but it has been suggested that nuclear topoisomerase VI could extent antagonistic effect of these two chloroplastic ROS on gene 1 actasanintegratorof O2-dependent signal in regulating nuclear expression (op den Camp et al., 2003; Gadjev et al., 2006; Laloi gene expression (Šimková et al., 2012). et al., 2007). Interestingly, the transcriptional response to apoplas- Apart from triggering PCD, the transcriptional reprogramming tic H2O2 produced during oxidative burst has little similarity to •− 1 of flu induces many genes of stress response and leads to rapid the effect of either chloroplastic O2 /H2O2 or chloroplastic O2 accumulation of SA, inducing a defense pathway characteristic of (Gadjev et al., 2006; Miller et al., 2009; Petrov et al., 2012; Sierla plant reaction to pathogens or wounding (Ochsenbein et al., 2006; et al., 2012). This illustrates a remarkable specificity of cellular Lee et al., 2007). One of the mechanisms triggering this pathway responses to different types and subcellular sources of ROS pro- exploits the calcium-sensing protein CAS localized to chloroplast duction. This also demonstrates the complexity of ROS signaling thylakoids (Figure 2). Regulation of CAS activity is linked to the and raises the question of the mechanisms responsible for such state of photosynthetic electron transfer chain. CAS has earlier specificity. been shown to be involved in high light acclimation of the green Clustering results of microarray experiments involving ROS alga Chlamydomonas reinhardtii (Petroutsos et al., 2011) and it is production in different subcellular compartments reveals distinct

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temporal signatures. For example, the gene expression profiles the transient protrusions of organellar surfaces that are known 4 h after elicitation with flg22 (a 22-amino acid fragment of the to be induced by stress, could be one of the mediators of this bacterial flagellar protein flagellin, which induces an apoplastic focused organellar cross-talk (Leister, 2012). Besides, all organelles oxidative burst via the activation of NADPH oxidase) have sim- move and dynamically associate with each other, and the role of ilarities to the profiles induced by ozone, while 12 h after flg22 this movement in stress response starts to be recognized (Suzuki treatment the expression profile resembled that of chloroplastic et al., 2012). For example, the bacterial elicitor harpin leads to HR ROS production induced by MV (Sierla et al., 2012). Ozone trig- accompanied by redistribution of mesophyll cell chloroplasts in gers generation of ROS in the apoplast, which leads to subsequent tobacco (Boccara et al., 2007). During the last 15 years the laws of chloroplastic ROS production and transcriptional up-regulation organellar movement have started to be revealed, but the conse- of 25 (out of 44) Arabidopsis CRK genes, but the activation profile quences of dynamic physical proximity and contact between the of these genes differs from that induced by high light (Wrzaczek organelles are unknown (Suetsugu et al., 2010; Sakai and Haga, et al., 2010). Thus, both temporal and spatial aspects appear to 2012). Recent studies demonstrate impairment of stress reactions be involved in determining the specificity of ROS. In addition, in the Arabidopsis mutants which are unable to move chloroplasts the outcome is most likely dictated by the specific combinations in response to light stimuli or to dock them to the plasma mem- •− 1 of ROS (O2 ,H2O2,or O2). It is unlikely that, for example, brane (Schmidt von Braun and Schleiff, 2008; Goh et al., 2009; merely a change in the cytoplasmic redox state could carry the Oliver et al., 2009; Lehmann et al., 2011). information about the subcellular source of H2O2. Therefore, as proposed (Møller and Sweetlove, 2010), the signal transduction CONCLUDING REMARKS would require specific and distinct sensory systems for the different Research performed over the last two decades has made it clear ROS in diverse subcellular compartments. that ROS signaling connects events that take place in very dif- The involvement of chloroplasts in plant systemic signaling has ferent subcellular locations, most importantly (but not limited also started to emerge recently (Joo et al., 2005; Szechyñska-Hebda to) the apoplast, the chloroplast, and the nucleus. To achieve the et al.,2010). Excessive illumination of Arabidopsis rosettes resulted elaborate and fine-tuned responses to biotic and abiotic stimuli in the propagation of an electric signal as measured by changes in that we observe on transcriptional, biochemical, and physiologi- plasma membrane potential of bundle sheath cells of leaf central cal level, intense and strictly controlled communication between veins. The signal was systemic, i.e., it also spread over the shaded the subcellular “crime scenes” must take place. While some com- leaves of the entire rosette. It correlated with transients of H2O2 ponents of this information exchange have been proposed, we still concentration and was altered in the mutant deficient in cytoso- lack a thorough understanding on how the apoplast, the chloro- lic APX2. Besides, the signal was deregulated by the inhibitors of plast, and the nucleus keep in touch. It will be perhaps one of the photosynthetic electron transfer and blocked by a Ca2+ channel major challenges of ROS research in plants to understand ROS- inhibitor. These observations suggest that information on light induced signaling pathways between different organelles. Once we conditions perceived by the chloroplast photosynthetic apparatus find out which components transmit information under specific is communicated to the cell, most likely through ROS production, conditions, we will be able to generate an integrated view of ROS and then propagated along the plant in a Ca2+-channel dependent signaling and its role in environmental adaptation. way (Szechyñska-Hebda et al., 2010). The possible integration of this pathway with a systemic NADPH oxidase-dependent signal ACKNOWLEDGMENTS (Miller et al., 2009) is the subject of further research. Research in the Plant Stress group of Professor Jaakko Kangasjärvi The high focused localization of ROS signaling events raises the is supported by Biocentrum Helsinki, the Academy of Finland, the issue of organelle spatial organization inside the cell. Stromules, University of Helsinki, and the ERA-PG.

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Citation: Shapiguzov A, Vainonen Sci. 3:292. doi: 10.3389/fpls.2012. Copyright © 2012 Shapiguzov, Vain- distribution and reproduction in other JP, Wrzaczek M and Kangasjärvi J 00292 onen, Wrzaczek and Kangasjärvi. This is forums, provided the original authors and (2012) ROS-talk – how the apoplast, This article was submitted to Frontiers in an open-access article distributed under source are credited and subject to any the chloroplast, and the nucleus get Plant Physiology, a specialty of Frontiers the terms of the Creative Commons copyright notices concerning any third- the message through. Front. Plant in Plant Science. Attribution License, which permits use, party graphics etc.

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