Reactive Oxygen Species in Plant Signaling

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Annual Review of Plant Biology

Annu. Rev. Plant Biol. 2018.69:209-236. Downloaded from www.annualreviews.org Access provided by Helsinki University on 05/28/18. For personal use only.

Reactive Oxygen Species in Plant Signaling Cezary Waszczak, Melanie Carmody, and Jaakko Kangasjärvi Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Centre, University of Helsinki, 00014 Helsinki, Finland; email: [email protected]

Annu. Rev. Plant Biol. 2018. 69:209–36

Keywords

First published as a Review in Advance on February 28, 2018

abiotic stress, plant–pathogen interactions, signal perception, signal transduction, long-distance signaling, stomatal closure, plant development

The Annual Review of Plant Biology is online at plant.annualreviews.org https://doi.org/10.1146/annurev-arplant-042817040322 c 2018 by Annual Reviews. Copyright All rights reserved

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Abstract As fixed organisms, plants are especially affected by changes in their environment and have consequently evolved extensive mechanisms for acclimation and adaptation. Initially considered by-products from aerobic metabolism, reactive oxygen species (ROS) have emerged as major regulatory molecules in plants and their roles in early signaling events initiated by cellular metabolic perturbation and environmental stimuli are now established. Here, we review recent advances in ROS signaling. Compartment-specific and cross-compartmental signaling pathways initiated by the presence of ROS are discussed. Special attention is dedicated to established and hypothetical ROS-sensing events. The roles of ROS in long-distance signaling, immune responses, and plant development are evaluated. Finally, we outline the most challenging contemporary questions in the field of plant ROS biology and the need to further elucidate mechanisms allowing sensing, signaling specificity, and coordination of multiple signals.

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Contents


1. INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. PRODUCTION, SCAVENGING, AND SIGNALING OF ROS . . . . . . . . . . . . . . . . 2.1. Chloroplasts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Peroxisomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Apoplast . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5. Transport of ROS Through Membranes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. ROS-SENSING MECHANISMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Oxidative Posttranslational Modifications of Cysteine Residues . . . . . . . . . . . . . . . 3.2. Oxidative Posttranslational Modifications of Methionine Residues . . . . . . . . . . . . 4. INTRACELLULAR INTERACTIONS BETWEEN ORGANELLE ROS AND REDOX SIGNALING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. How Is Signaling Specificity Retained in the Cytosol? . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Chloroplast-Mitochondrion Crosstalk, Signaling, and PAP . . . . . . . . . . . . . . . . . . . 5. APOPLASTIC AND ORGANELLE ROS INTERACTIONS DURING STRESS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Cell-to-Cell ROS Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. ROS in Plant Immunity and Stomatal Closure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. ROS IN PLANT DEVELOPMENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. INTRODUCTION

Singlet oxygen (1 O2 ): oxygen molecule in which the two highest-energy electrons have opposite spin and are paired, in contrast to triplet oxygen (3 O2 )

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The evolution of multicellular life forms has been shaped by the oxygen-rich atmosphere (113). In the presence of oxygen, cellular processes characterized by high rates of electron or energy transfer inevitably lead to the formation of reactive oxygen species (ROS) by electron or energy leakage to molecular oxygen (O2 ). Additionally, multiple enzymatic reactions have evolved to produce ROS either as a primary product or as a by-product. ROS are defined as oxygen-containing molecules exhibiting higher chemical reactivity than O2 . In plants, the major forms of ROS are singlet oxygen (1 O2 ), superoxide anion (O2 ·− ), hydrogen peroxide (H2 O2 ), and hydroxyl radical (HO· ) (Figure 1). The potential for cellular damage from enhanced production of these molecules has been alleviated through evolutionary pressure to develop and expand a range of enzymatic and nonenzymatic ROS scavengers (Figure 2). Rapid changes in compartmental redox balance and ROS homeostasis are among the earliest symptoms following fluctuations in environmental conditions. Plants monitor these parameters and utilize them as signals in multiple processes that serve to adjust metabolism or physiology either at the whole plant or tissue level or in specific subcellular compartments.

2. PRODUCTION, SCAVENGING, AND SIGNALING OF ROS Compartmentalization of production and scavenging determines the biological functions of ROS in plants. In particular, O2 ·− , H2 O2 , and HO· can be produced in nearly every subcellular compartment. Consequently, with the exception of the apoplast, which has a low antioxidant capacity, each production site is equipped with an array of antioxidant systems to buffer the local redox environment (reviewed in 49, 103). The concentration and longevity of ROS are determined by Waszczak

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Figure 1 ∗

Generation and chemical structures of reactive oxygen species. Electrons are depicted as dots. Abbreviations: 3 P680 , triplet state of the primary electron donor of photosystem II; SOD, superoxide dismutase.

the composition and availability of antioxidant systems. The estimated lifetime for HO· , the most reactive form of ROS, is of the order of nanoseconds, and for 1 O2 microseconds. The lifetimes of H2 O2 —the most stable form of ROS—and O2 ·− are considerably longer (milliseconds to seconds) and depend largely on the presence and activity of dedicated ROS scavengers (87). During the past few decades the concept of oxidative stress, in which ROS were regarded as harmful substances that indiscriminately oxidize various molecules and structures, has changed to the concept of ROS signaling (48, 66). According to current understanding, effective antioxidative systems in the symplastic compartments keep ROS concentrations low even under increased ROS production rates (49, 103). Therefore, any elevation in ROS concentration in different subcellular compartments appears to be transient, reflecting the efficiency of scavenging systems. The higher production rates provoke a shift in the compartmental redox balance toward a more oxidized state, which can be sensed by various compartment-specific systems to regulate gene expression. In the following sections we review and give selected examples and concepts of how ROS are formed, scavenged, and act as signaling molecules in the major cellular compartments.

2.1. Chloroplasts Chloroplastic ROS production is tightly associated with light-dependent photosynthetic reactions, and increased ROS production serves as a marker of changing internal or external conditions that require the acclimation or adjustment of metabolism. Below we review the most important chloroplastic ROS sources and the signal transduction events that mediate these plant–environment interactions. 2.1.1. Chloroplastic ROS production. Unique to chloroplasts is the formation of nonradical, highly reactive 1 O2 (Figure 2). The singlet state of oxygen is generated within thylakoid mem∗ branes mainly by energy transfer from the triplet state of the primary electron donor (3 P680 ) of photosystem II to ground state molecular oxygen (3 O2 ) (Figure 1) (46). No direct enzymatic scavengers of 1 O2 have evolved. Instead, scavenging of 1 O2 occurs primarily through reactions with other molecules, particularly carotenoids (111), tocopherols (76), and membrane lipids (44). Recent studies have extended our knowledge of 1 O2 -induced cleavage of β-carotene, in which βcyclocitral and other breakdown products are involved in 1 O2 -related chloroplast retrograde signaling (112). For more details on 1 O2 signaling, readers are directed to recent reviews (17, 29, 81). www.annualreviews.org • Reactive Oxygen Species

Carotenoids: organic pigments produced by plants and algae

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Figure 2 Production and scavenging of ROS. Formation of singlet oxygen occurs mainly by the transfer of energy from the triplet state of the ∗ primary electron donor (3 P680 ) of PSII to the ground state triplet oxygen. Superoxide anions arise during processes characterized by high rates of electron flow, such as mitochondrial and chloroplastic electron transport chains, and as a result of multiple enzymatic reactions. Production of hydrogen peroxide results from enzymatic and spontaneous dismutation of superoxide anions and activity of glycolate oxidases. With the exception of the apoplast, subcellular compartments possess various nonenzymatic and enzymatic ROS scavengers that under optimal growth conditions keep ROS concentrations very low. Hydrogen peroxide might cross biological membranes via aquaporins. In the inner membrane, boxes I–V represent complexes of the mitochondrial electron transport chain. ∗ Abbreviations: 3 P680 , triplet state of the primary electron donor of photosystem II; AOX, alternative oxidase; APX, ascorbate peroxidase; ASC, ascorbate; CAT, catalase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; Fd, ferredoxin; FNR, ferredoxin-NADP+ reductase; FTR, ferredoxin-dependent thioredoxin reductase; GOX, glycolate oxidase; GR, glutathione reductase; GPXL, glutathione peroxidase-like; IMS, intermembrane space; MDA, monodehydroascorbate; MDAR, monodehydroascorbate reductase; NTR, NADPH-dependent thioredoxin reductase; NTRC, NADPH-dependent thioredoxin reductase C; OPPP, oxidative pentose phosphate pathway; PAO, polyamine oxidase; PRX, peroxidase; Prxr, peroxiredoxin; PSI/II, photosystem I/II; RBOH, respiratory burst oxidase homolog; ROS, reactive oxygen species; SA, salicylic acid; SOD, superoxide dismutase; TRX, thioredoxin; XO, xanthine oxidase.

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One-electron reduction of oxygen at PSI produces the moderately reactive O2 ·− (Figure 1, Figure 2), which is dismutated into H2 O2 on the stromal side of the thylakoid membrane spontaneously or enzymatically via superoxide dismutases (SODs) (3). Chloroplast SODs include iron-SODs (FeSODs) and copper/zinc-SODs (Cu/ZnSODs), and they are crucial for chloroplast function and development. In chloroplast stroma H2 O2 is detoxified by ascorbate peroxidases (APXs), glutathione peroxidase-like (GPXLs) enzymes, and peroxiredoxins (Prxrs) (3). The flow of electrons from water through the photosynthetic electron transport chain and via O2 ·− to H2 O2 and then back to water serves as a sink for excess electrons (water-water cycle). This classical model has been recently extended by the discovery of the photoprotective role of 2-Cys Prxrs acting synergistically with thylakoid APX under high-light conditions (5). Prxrs use thiol-based catalytic mechanisms to reduce H2 O2 (35). Regeneration of Prxrs can be catalyzed by thioredoxins (TRXs), glutaredoxins (GRXs), and NADPH-dependent thioredoxin reductase C, a two-domain enzyme exhibiting both thioredoxin reductase and TRX activity (35). TRXs are reduced by NADPH-dependent thioredoxin reductases and ferredoxin-dependent thioredoxin reductases (118). 2.1.2. Chloroplastic ROS and redox signaling. Chloroplastic formation of H2 O2 and consequent alterations in the status of chloroplast antioxidant systems have been recognized as parameters providing information about environmental and metabolic changes to the nucleus in chloroplast retrograde signaling (reviewed in 17, 29, 81). As a simple and ubiquitous molecule, H2 O2 does not carry any information about its origin. Therefore, an outstanding problem in the role and significance of H2 O2 as a retrograde signal has been the question of specificity—how can the nucleus differentiate H2 O2 produced in different subcellular compartments, all of which potentially affect the concentration of H2 O2 in the cytoplasm? This key issue is discussed further in Section 4.1. Recent reports of chloroplastic ROS transport and signal transduction to the nucleus have presented evidence for (a) direct stromule-mediated delivery of ROS and proteins to the nucleus; (b) fast regulation of nuclear H2 O2 concentration by a population of companion chloroplasts localized around the nucleus; and (c) signaling via accumulation of chloroplast metabolites, their oxidative derivatives, or both (Figure 3). Stromules are dynamic plastid projections thought to maintain direct links between a small number of plastids and nuclei (40, 53). Stromule formation in vivo was rapidly induced with chemicals that cause chloroplastic ROS generation and have been linked to the light-dependent chloroplast redox status (14). Regulation can be independent from the cellular environment, as isolated chloroplasts can also form stromules (14). Whereas rapid stromule induction was observed 1 h after exogenous H2 O2 and salicylic acid (SA) treatments, slower reactions have been observed after 22–48 h in response to bacterial effectors (15), most likely related to the onset of the hypersensitive response. Importantly, stromules are capable of protein (15, 53) and H2 O2 (15) transport—bypassing a long transit through the cytosol. In addition, H2 O2 produced in chloroplasts in a light-dependent manner can be transferred to nuclei with no apparent stromule formation from a subpopulation of chloroplasts closely surrounding the nucleus (43). This finding agrees with an earlier report showing that an increase in localized H2 O2 production induced by application of a 405-nm laser to chloroplasts adjacent to nuclei resulted in the transfer of H2 O2 to the nucleus (15). Such a transfer of ROS is believed to regulate the expression of high-light-responsive genes and could be incorporated into existing signaling models to explain how ROS signals can reach the nucleus. Chloroplastic ROS production also affects nuclear gene expression indirectly. ROSdependent oxidative posttranslational modifications of chloroplast catabolic enzymes increase the

www.annualreviews.org • Reactive Oxygen Species

APX: ascorbate peroxidase GPXL: glutathione peroxidase-like Prxr: peroxiredoxin TRX: thioredoxin GRX: glutaredoxin SA: salicylic acid Hypersensitive response: controlled death of cells surrounding the place of infection to limit the spread of pathogens

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concentration of metabolites that have a signaling function. The chloroplastic 3 phosphoadenosine 5 -phosphate (PAP) phosphatase SAL1 undergoes redox- or H2 O2 -dependent oxidative inactivation (16). This leads to the accumulation of PAP, which is suggested to act as a second messenger conveying the information about chloroplast redox status to the nucleus (41). In the context of signaling specificity, it would be of interest to investigate whether signaling events initiated by direct H2 O2 translocation from chloroplasts to nucleus, which most likely modify the activity of nuclear redox-regulated transcription factors (36), interact with PAP-dependent signaling. Both PAP-dependent signaling and transcription regulation would be downstream of chloroplastic H2 O2 production. The delivery of chloroplastic H2 O2 directly to the nucleus does not seem to provide sufficient information because from the nuclear perspective a specificity factor that could differentiate, e.g., chloroplastic and peroxisomal H2 O2 , would be missing. Could PAP be such a specificity factor? This is discussed further in Section 4.2. Apoplast red

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Figure 3 (Figure appears on preceding page) ROS signaling processes. Information from elevated ROS concentrations or altered compartmental redox balance resulting from activity of ROS-scavenging systems is rapidly transferred to the nucleus and triggers adaptation or acclimation mechanisms. The initial ROS-sensing events are mediated by ROS- and redox-sensitive proteins or direct oxidative damage of cellular metabolites, e.g., β-carotene. Accumulation of ROS within the apoplast triggers a rapid increase in cytosolic Ca2+ . The apoplastic ROS-sensing mechanisms as well as the identity of ROS-dependent Ca2+ channels are currently not known. Elevated production of ROS in the chloroplast leads to accumulation of PAP, which acts as a secondary messenger conveying the information about the redox status within the organelle. In consideration of the dual localization of the PAP catabolism enzyme SAL1, it can be assumed that a similar process can occur in the mitochondria. Perturbed mETC triggers nuclear import of mobile transcription factors located in the ER that are negatively regulated by the RCD1 transcriptional coregulator. RCD1 is necessary for part of the transcriptomic responses to altered chloroplast and mitochondrial redox balance. SA-mediated inactivation of peroxisomal CAT leads to inhibition of JA and IAA biosynthesis and alters the cytoplasmic glutathione redox status. H2 O2 might be transported to the nucleus via stromules and from subpopulations of chloroplasts surrounding the nucleus. Nuclear ROS accumulation likely changes the activity of multiple ROS- and redox-sensitive transcription factors. Abbreviations: 2CPA, 2-CYS PEROXIREDOXIN A; ANAC, ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN; AOX, alternative oxidase; ASC, ascorbate; CAS, CALCIUM SENSOR; CAT, catalase; ER, endoplasmic reticulum; GRI, GRIM REAPER; GSH, glutathione; IAA, indole-3-acetic acid; JA, jasmonic acid; MC9, METACASPASE9; MDS, mitochondrial dysfunction stimulon; MEcPP, methylerythritol cyclodiphosphate; mETC, mitochondrial electron transport chain; PAP, 3 -phosphoadenosine 5 -phosphosulfate; PRK5, POLLEN RECEPTOR LIKE KINASE5; RAP2.4a, RELATED TO APETALA-2.4a; RCD1, RADICAL-INDUCED CELL DEATH1; ROS, reactive oxygen species; SA, salicylic acid; SOT12, SULFOTRANSFERASE12; XRN, exoribonuclease.

2.2. Mitochondria In photosynthetic tissues, the contribution of mitochondria to total cellular ROS production is relatively low. However, mitochondrial redox balance can serve as an indicator of multiple environmental cues and is intrinsically linked to the chloroplast function. In the following section we analyze how mitochondrial redox status contributes to regulation of gene expression. 2.2.1. Mitochondrial ROS production. Mitochondrial ROS production is tightly associated with the mitochondrial electron transport chain (mETC), located in the inner mitochondrial membrane. Mitochondrial complexes I, II, and III are believed to be the major sources of O2 ·− production; however, the relative importance of these production sites is difficult to assess and most information is derived from animal mitochondria (55). Complexes I and II produce O2 ·− at the matrix side of the inner mitochondrial membrane (Figure 2). In animal mitochondria, complex III produces O2 ·− on both sides of the inner mitochondrial membrane (8). Because there are no major differences between plant and animal complex III, it can be assumed that O2 ·− production on both sides of the inner mitochondrial membrane occurs in plants (Figure 2). Thus, ROS in the intermembrane space (IMS) could have a signaling function in plants similar to that in animals (8). It is not clear whether the IMS has enzymatic ROS scavengers; however, in consideration of the permeability of the outer mitochondrial membrane, O2 ·− dismutation and H2 O2 quenching could depend on cytoplasmic components. Additionally, because the last step of ascorbate (ASC) biosynthesis takes place in the mitochondrial IMS, O2 ·− could be scavenged directly by reduced ASC and thus alter the ASC redox state, which could act as a signal. Within the mitochondrial matrix O2 ·− is dismutated to H2 O2 either spontaneously or via the mitochondrial manganeseSOD; subsequently, H2 O2 is scavenged by Prxrs (45) and APX, because a full set of enzymes necessary for completion of the ascorbate-glutathione (ASC-GSH) cycle have been localized to plant mitochondria (22). 2.2.2. Mitochondrial ROS and redox signaling. Plants have strategies to avoid mitochondrial ROS formation. Electron flow is redirected through an alternate pathway bypassing the www.annualreviews.org • Reactive Oxygen Species

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complexes III and IV (55). Alternative oxidases (AOXs) have a major role in this redirection upstream of complex III when, for example, functioning of complex III is suboptimal. Although no major impacts on development, physiology, or metabolism have been reported for AOX mutants grown under favorable conditions (131), AOX is indispensable under conditions that cause mitochondrial redox imbalance (50). Stress conditions perturbing mETC activate AOX by reducing the AOX dimer and by increasing the expression of genes that encode AOX and several other mitochondria-targeted proteins (mitochondrial dysfunction stimulon, MDS) through mitochondrial retrograde signaling, most likely in response to complex III–derived ROS (28, 102). A subsequent increase in AOX activity directs electrons to O2 before complex III to alleviate ROS formation and counteract the altered redox imbalance. The execution of this process involves two endoplasmic reticulum (ER)-localized transcription factors ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN13 (ANAC013) (28) and ANAC017 (102), which are thought to translocalize to the nucleus in response to organelle-dependent stress signals. Recent results on chloroplast-mitochondrion crosstalk are discussed further in Section 4.2.



2.3. Peroxisomes Peroxisomes host multiple metabolic processes, many of which lead to formation of ROS. In this section we review factors shaping the peroxisomal ROS pool and present the most recent findings in peroxisomal ROS signaling. 2.3.1. Peroxisomal ROS production. Under the current concentration of CO2 in the atmosphere a significant proportion of RuBisCO catalytic cycles result in oxygenation rather than carboxylation of ribulose-1,5-bisphosphate. The resulting 2-phosphoglycolate is metabolized to glycolate and transported to peroxisomes, where it undergoes glycolate oxidase–dependent oxidation to glyoxylate with concomitant production of H2 O2 (Figure 2). In photosynthetically active tissues, peroxisomal ROS production is tightly linked to photosynthesis and accounts for most of the ROS produced (49). However, because peroxisomes have a potent H2 O2 -scavenging system, flux through the photorespiratory pathway does not necessarily translate into an increase in H2 O2 content. Catalases (CATs) are major peroxisomal H2 O2 scavengers, and mutant plants deficient in CAT activity exhibit severe growth abnormalities dependent on photoperiod, light intensity, and CO2 concentration (110). Despite the relatively low affinity for H2 O2 , CATs can efficiently remove photorespiratory H2 O2 and keep the estimated peroxisomal H2 O2 concentrations below 10 μM (49). Whereas the existence of peroxisomal APX and ASC-GSH cycle enzymes has been demonstrated for multiple species (31), no phenotypes have been observed in Arabidopsis plants deficient in peroxisomal APX3 (101), possibly indicating a relatively low contribution to the peroxisomal antioxidant system. 2.3.2. New concepts in peroxisomal ROS and redox signaling. The paradigm of a purely metabolic function for peroxisomal H2 O2 scavenging is slowly changing. Peroxisomal ROS levels, closely regulated by CAT activity, are now emerging as a source of signals, with most information originating from the analysis of Arabidopsis plants deficient in CAT2, the primary peroxisomal H2 O2 scavenger (110). Disruption of photorespiratory H2 O2 scavenging combined with exposure to photorespiration-promoting conditions shifts the redox status of the cellular GSH and ASC pool toward a more oxidized state (110), coinciding with rapid transcriptome reprogramming (70, 110). However, under steady-state conditions little or no increases in H2 O2 concentration could be observed in cat2 mutants (92), possibly owing to low glycolate oxidase activity (70) combined with the antioxidant function of cytoplasmic H2 O2 -scavenging enzymes (137). This finding suggests 216

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that some of the phenotypes observed in cat2 plants might be related to perturbed glycolate metabolism or altered cytoplasmic redox balance rather than H2 O2 buildup. The efficiency of CATs raises a crucial question about the signaling role of photorespiratory H2 O2 . Can CAT activity decrease to allow transient H2 O2 accumulation? Recent results suggest that this could take place at least during SA signaling in plant-pathogen interactions (Figure 3). Following the seminal study demonstrating that binding of SA to CAT decreased its activity (20), Yuan et al. (153) showed that SA-mediated inhibition of peroxisomal H2 O2 scavenging inhibits auxin and jasmonic acid (JA) biosynthesis to increase the resistance to biotrophic pathogens. This finding agrees with earlier reports that describe increased resistance of cat2 plants to biotrophic bacteria (18). At the molecular level, inhibition of auxin biosynthesis was related to sulfenylation and deactivation of TRYPTOPHAN SYNTHETASE β SUBUNIT1 (TSB1), which delivers precursors for auxin biosynthesis, and inhibition of JA synthesis was attributed to the requirement of CAT for the activity of peroxisomal acyl-CoA oxidases ACX2 and ACX3 (153). TSB1 is located in the chloroplast stroma; therefore, the regulation of TSB1 activity is likely related to secondary effects following the decrease in CAT activity, e.g., altered chloroplast redox status. Furthermore, this could mean that any treatment resulting in chloroplastic redox imbalance might affect TSB1 activity, as from the chloroplast perspective it is difficult to differentiate between internal and external ROS and redox signals. In addition to inhibition by SA, CAT activity can be regulated by many other factors. Increases in cytoplasmic Ca2+ were rapidly followed by a Ca2+ rise in peroxisomes (25), which promoted CAT activity possibly via Ca2+ -dependent interactions between CAT and calmodulin (150). Optimal CAT function was maintained by the chaperone NO CATALASE ACTIVITY1 (82), providing another mode of regulation for its activity. NUCLEOREDOXIN1, a pathogeninducible oxidoreductase, was found to be a crucial determinant of CAT function (74). Another factor contributing to an increase in the rate of peroxisomal ROS production could be the activity of cytosolic glyoxylate reductase (GLYR1 in Arabidopsis), which reduces glyoxylate back to glycolate, potentially enabling its peroxisomal uptake for reoxidation. Recently, Denecker et al. (33) demonstrated that introduction of the glyr1 mutation into the cat2 background improved the survival of the double mutant under conditions promoting photorespiration.

JA: jasmonic acid

2.4. Apoplast The apoplast serves as an interface for the exchange of nutrients and signals between plant cells and the environment. In many cases, plant responses to environmental and endogenous stimuli involve the accumulation of ROS within this compartment. Here, we review the most prominent production mechanisms and signaling roles of apoplastic ROS. 2.4.1. Apoplastic ROS production. In contrast to intracellular sources, apoplastic ROS production results from active stimulation of ROS-producing enzymes such as apoplastic peroxidases, polyamine oxidases (PAOs), and plasma membrane-localized NADPH oxidases (respiratory burst oxidase homologs, RBOHs) (Figure 2) (64, 73, 119). The role of apoplastic peroxidases as ROS producers was initially shown pharmacologically (86) and later by silencing (7) or generating stable mutant lines (27), which established two Arabidopsis peroxidases, PRX33 and PRX34, as key enzymes contributing to the apoplastic ROS burst in biotic stress. However, although accumulating evidence supports the importance of apoplastic peroxidases especially in plant immunity, little is known about the molecular mechanisms that regulate the activity of these enzymes. PAOs catalyze catabolism of spermidine and spermine with concomitant production of H2 O2 . The PAO-generated H2 O2 plays a role under biotic (151, 152) and abiotic stress conditions (98), www.annualreviews.org • Reactive Oxygen Species

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as well as in plant development (126). Multiple lines of evidence suggest that polyamine availability is a major factor contributing to the regulation of H2 O2 production by PAOs. NADPH oxidases, which are perhaps the most important class of apoplastic ROS producers, transfer electrons across the plasma membrane from cytoplasmic NADPH to molecular oxygen to produce O2 ·− . The Arabidopsis genome contains 10 genes for the RBOH isoforms (A–J) (123). Most ROS signaling during abiotic and biotic stress relies on the activity of two partially redundant isoforms, RBOHD and RBOHF (64, 77, 94, 129, 130); some of the other isoforms are involved in the regulation of plant development (discussed in Section 6). In contrast to the activity of apoplastic peroxidases, the molecular mechanisms regulating the activity of NADPH oxidases are relatively well understood and involve transcriptional (97) and posttranslational regulation (64, 73, 119). The O2 ·− formed in the apoplast can be dismutated to H2 O2 either spontaneously or by apoplastic SODs. In Arabidopsis, the identity of apoplastic SODs remains unknown, even though indirect evidence suggests their existence. None of the seven canonical SODs possess a secretory signal peptide, but some are found in the extracellular space following activation of a SA-induced secretory pathway (21). Two putative SODs, AT3G56350 and AT4G00651, are predicted to be secreted; however, the function of these proteins remains to be determined. Intriguingly, compared with the intracellular environment, the apoplast is maintained in a relatively oxidized state and is estimated to contain most of the leaf H2 O2 (see 49 and 103 for the estimates) while containing low concentrations of ASC and GSH. The apoplastic metabolism of these compounds clearly has implications for cellular metabolism, including acclimation of photosynthesis to fluctuating light (68); however, it is not clear whether this is related to their antioxidant functions. 2.4.2. Ozone as a tool for investigating apoplastic ROS. Whereas the accumulation of ROS in the apoplast serves to coordinate local responses, such as execution of cell death, in plant-microbe interactions, early apoplastic ROS accumulation probably serves as a signal to neighboring or distal cells. Therefore, it is crucial to recognize and separate the signaling events triggered by ROS accumulation within the apoplast from those dependent on local recognition of microbe-associated molecular patterns (MAMPs), although these processes might not be completely independent (73). Such approaches might focus on signaling events initiated by perception of MAMPs in rboh mutants (148) that identify ROS-independent responses, or utilize apoplastic ROS donors such as ozone (O3 ) to investigate ROS-dependent responses (134). O3 enters plant tissues through stomata, decomposes in the cell walls to various ROS, and triggers active ROS generation—ultimately leading to the formation of hypersensitive response-like cell death (67, 134). Application of O3 as an experimental tool effectively mimics the intrinsic ROS burst specific to the apoplast. Unlike other methods, it can be applied noninvasively at a precise concentration and duration (67, 134) and has been described as maybe the most environmentally relevant way to probe the function of ROS in signaling processes (103). Among the first events following accumulation of apoplastic ROS is the activation of H2 O2 -dependent Ca2+ channels, which mediate the influx of apoplastic Ca2+ into the cytoplasm (107). The identity of these channels remains elusive still and presents a major challenge in understanding apoplastic ROS signaling. Other early responses include accumulation of ethylene (134); however, the regulation of most O3 responsive transcripts is independent of ethylene, as well as SA and JA, signaling (147), suggesting the existence of ROS-dependent apoplast-to-nucleus signaling pathways independent from hormonal signaling. 2.4.3. Sensing of ROS within the apoplast. The signaling function of apoplastic ROS was suggested over 20 years ago (67) and is now well established (64, 73, 119, 123). However, the initial processes in apoplastic ROS perception, as well as in other subcellular compartments, are still unresolved. In view of compartment-specific ROS signaling, mechanisms for apoplastic ROS sensing

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proposed thus far (73, 119) assume the existence of local signaling components that monitor the apoplastic redox status. These mechanisms include sensing of apoplastic H2 O2 or redox status via specialized sensors that could detect ROS, e.g., directly via oxidative posttranslational modifications (PTMs) or indirectly through oxidized apoplastic proteins, metabolites, or both (Figure 3; discussed in Section 3). The apoplast contains a number of cysteine-rich peptides (127) that could participate in ROS sensing. Another group of proteins that function in processes related to apoplastic ROS accumulation are cysteine-rich receptor-like kinases (CRKs) (11). Evidence supporting their possible role in apoplastic ROS sensing includes (a) the presence of conserved cysteines in the ectodomain, (b) transcriptional regulation in response to apoplastic ROS (145), and (c) a functional analysis of crk mutant plants (11). Additionally, according to publicly available interactome data (62), a set of CRKs interact with RBOHs. Furthermore, emerging evidence indicates cysteine-dependent function of CRKs (149); however, it remains unclear whether these residues are involved in signaling processes or have structural functions. The existence of local perception mechanisms has been recently supported by the discovery of downstream processes involved in the regulation and progression of O3 -induced cell death, which relies on RBOHD, an apoplastic cysteine-rich protein GRIM REAPER (GRI), and a receptor-like kinase (RLK), POLLEN RECEPTOR LIKE KINASE5 (PRK5), which together may form an apoplastic signaling module (144, 146). Cleavage of the GRI preprotein by METACASPASE9 resulted in a 12-amino-acid GRI peptide that bound to its receptor PRK5 to initiate the onset of ROS-dependent cell death (146). The whole process was dependent on ROS produced by RBOHD, but whether ROS were acting on GRI, involved in the activation of METACASPASE9, or required for the interaction of the short peptide ligand with PRK5 is unknown.

Ectodomain: the apoplastic domain of plasma membrane–localized protein Dipole moment: a measure of molecule polarity HyPer: genetically encoded H2 O2 sensing probe

2.5. Transport of ROS Through Membranes Another line of evidence supports intracellular perception of apoplastic ROS. The dipole moment of H2 O2 is larger than that of H2 O, preventing free diffusion through membranes. However, according to studies of yeast survival, multiple plant aquaporins can transport H2 O2 (reviewed in 6). Following these initial discoveries, Costa et al. (25) demonstrated that extracellular supplementation of H2 O2 to plant cells expressing a cytoplasmic HyPer probe provoked accumulation of H2 O2 within the cytoplasm with no apparent delay, indicating rapid transfer through the plasma membrane. The H2 O2 permeability of biological membranes was also demonstrated in chloroplastic ROS signaling, because even under low-light intensities a fraction of chloroplastic ROS leaked or was transported from the chloroplast to the cytosol (100). Finally, the aquaporin PLASMA MEMBRANE INTRINSIC PROTEIN1;4 (PIP1;4) imported apoplastic ROS during plant-pathogen interactions (128) and PIP2;1 was suggested to mediate H2 O2 transport in guard cell signaling (51). Mechanisms for apoplastic and cytosolic perception of apoplastic ROS likely coexist to fine-tune cellular responses. However, intracellular sensing of apoplastic ROS raises questions related to ROS signaling specificity (see Section 4.1 and the sidebar titled Are Tissueand Organ-Resolution ROS Concentration Measurements Biologically Relevant?).

3. ROS-SENSING MECHANISMS At the molecular level the biological roles of ROS are dictated largely by their ability to react with a broad range of proteins and metabolites as well as by their consumption of reducing equivalents by the ROS-scavenging machinery. Most ROS-sensing mechanisms are thought to use the oxidizing properties of ROS. The initial ROS-sensing events include oxidative PTMs of sensory proteins and oxidation of metabolites. Additionally, the activity of ROS-scavenging enzymes shifts the redox www.annualreviews.org • Reactive Oxygen Species

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ARE TISSUE- AND ORGAN-RESOLUTION ROS CONCENTRATION MEASUREMENTS BIOLOGICALLY RELEVANT? In many published articles, ROS concentration from whole leaf and organ samples has been measured by several different methods. However, recent results indicate that such measurements, apart from being highly dependent on the techniques (see 103 for a detailed description of critical issues in ROS measurements), might not be biologically relevant in the context of ROS signaling. Tissue-level ROS measurements average the steady-state ROS levels of the whole cell, neglecting compartment-specific differences (49); thus, these measurements cannot give meaningful information about the changes at the subcellular level, which can have important implications for signaling function. Furthermore, experiments that use the membrane-anchored HyPer genetically encoded H2 O2 sensor indicate the existence of discrete ROS maxima and a limited ROS diffusion distance (95). Such spatial distribution of ROS might be explained by a local downregulation of cellular antioxidant mechanisms that enables controlled accumulation of ROS, triggering downstream signaling processes (142, 143). Therefore, in order to gain more information about the physiological relevance of ROS signaling, the application of nondiffusible ROS sensors at a subcellular resolution is necessary (139). The question about localized ROS sensing gains additional importance in the context of the heterogeneous environment within subcellular compartments, e.g., the plasma membrane (60).

status of electron donors such as NADPH, GSH, or ASC toward a more oxidized state. Importantly, not all responses mentioned above can be attributed to signaling, especially if ROS accumulation has been artificially increased in mutant backgrounds or by the application of external stimuli.

3.1. Oxidative Posttranslational Modifications of Cysteine Residues PTMs of proteins can alter the function or stability of proteins by adding covalent functional groups or by other modifications that affect protein properties. Phosphorylation, glycosylation, and ubiquitinylation are well-known examples of such PTMs. ROS and altered cellular redox balance can also directly affect a number of proteins which have signaling function that leads to changes in cellular acclimation as a response to changes in the surrounding environment. Sulfur atoms in cysteine and methionine residues are the primary targets for H2 O2 -dependent oxidative PTMs of ROS-sensitive proteins.

pKa : logarithmic derivative of the acid dissociation constant; negatively correlates with the ability of acid to dissociate

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3.1.1. Factors determining reactivity of cysteine residues. Reaction of H2 O2 with the cysteine thiolate anion (-S− ) leads to the formation of cysteine sulfenic acid (-SOH). Unless stabilized within the protein environment, -SOH reacts with either GSH, leading to protein S-glutathionylation (-SSG), or other thiol groups, resulting in the formation of intra- or intermolecular disulfide bonds (-S-S-). Under high concentrations of H2 O2 , or when the protective thiols are not available, -SOH can undergo further oxidation to sulfinic (-SO2 H) and sulfonic (-SO3 H) acid, which in most cases leads to protein damage (117). Waszczak et al. (140) identified approximately 100 sulfenylated cytosolic proteins in plant cells treated with H2 O2 ; therefore, it can be assumed that sulfenylation is a widespread PTM. With the exception of sulfonylation, oxidative PTMs of cysteine residues are reversible. Deglutathionylation and reduction of disulfide bonds are catalyzed by GRXs and TRXs, which form large multigene families (91). Reduction of sulfinic acid can be catalyzed by sulfiredoxins; however, in Arabidopsis this mechanism has been described only for chloroplastic and mitochondrial Prxrs (56, 114). Within ROS-sensitive proteins the susceptibility of cysteine residues to react with H2 O2 is not equal and is determined largely by the local electrostatic environment affecting cysteine residue pKa . For example, relatively nonreactive cysteine thiol Waszczak

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groups (-SH) are more prone to oxidation in their activated thiolate anion (-S− ) form; therefore, the local pH largely determines the susceptibility of cysteine residues to oxidation (116). 3.1.2. ROS or redox signaling? GRXs and TRXs, which reduce multiple forms of cysteine oxidative PTMs, are selective toward their target proteins (118) and their reactivity is determined largely by the availability of reducing equivalents, GSH and reduced ferredoxin (Fdred ) or NADPH. Therefore, conditions that limit the abundance of electron donors, e.g., darkness for Fdred or activity of the GSH-ASC cycle for GSH, ultimately limit the function of GRXs and TRXs. Thus, the status of oxidative PTMs of cysteine residues is a result of H2 O2 concentration (usually termed ROS signaling) and the availability of reducing equivalents (usually termed redox signaling). Although these two mechanisms might be connected, redox signaling is a much broader process because it does not necessarily result from increased ROS concentrations at the site of signal perception. An example of such signaling is the light-dependent reducing activation of Calvin cycle enzymes by the ferredoxin-TRX redox relay (118). Another example was recently demonstrated with a redox-sensitive roGFP2 probe, constructed by introducing cysteine residues into the nascent green fluorescent protein (GFP) sequence to enable the formation of a redox-dependent disulfide bond that influences the GFP emission spectra (37). Later, it was discovered that the in vitro oxidation of roGFP2 by H2 O2 is a slow process, and in plants the fast in vivo response results from GRX-mediated reduction or formation of disulfide bonds within roGFP2. Therefore, the roGFP2 probe responds to cellular redox changes by monitoring the GSH/GSSG ratio (90). Results obtained with this system suggest that GRXs might serve as a sensor of the GSH redox status and target host proteins for signaling purposes. The two examples listed above indicate that altered compartmental redox balance might change the activity of multiple enzymes and signaling proteins, even when the target proteins are distant from the site of ROS formation.

Green fluorescent protein (GFP): emits fluorescence when exposed to light of certain wavelengths Rate constant: measure of chemical reaction rate

3.1.3. Two-step ROS-sensing mechanisms. In the context of ROS signaling, emerging evidence indicates that oxidation of cysteine residues within the target proteins might be catalyzed by specialized ROS-scavenging enzymes such as Prxrs or GPXs characterized by extremely high rate constants for reactions with H2 O2 , enabling perception of physiological ROS concentrations. Upon oxidation, these sensor proteins interact with and oxidize effector proteins, forming a redox relay. Thus far, the only example of such a redox relay in plants has been described for the GLUTATHIONE PEROXIDASE-LIKE3 (GPXL3)–ABA-INSENSITIVE2 (ABI2) H2 O2 -sensing system, which has been suggested to control stomatal closure (93). In vitro, GPXL3 underwent H2 O2 -dependent oxidation and interacted with and oxidized ABI2, ultimately inhibiting its activity (93). However, recent data suggest that such interaction is unlikely in planta as GPXL3 localizes to the ER membrane with its catalytic domain facing the ER lumen (4), whereas ABI2 is a cytoplasmic protein. It remains to be elucidated whether ABI2 interacts with other GPXLs or other specialized H2 O2 sensors and whether it is able to directly sense H2 O2 as demonstrated in vitro (88). Analogous redox relay mechanisms in yeast have been described, in which the thiol peroxidase GPX3 oxidizes the transcription factor YAP1, ultimately leading to its nuclear import and transcriptional activity (32). In humans, Prxr-2 oxidizes the transcription factor STAT3, leading to its inactivation (120). Because cysteine thiols in most proteins are less susceptible to oxidation than those of thiol peroxidases, it is likely that many direct ROS-sensing mechanisms can utilize similar signaling principles.

3.2. Oxidative Posttranslational Modifications of Methionine Residues In addition to cysteine thiols, methionine residues can be subject to oxidative PTMs. Reaction of H2 O2 with methionine residues (-S-CH3 ) leads to the formation of methionine www.annualreviews.org • Reactive Oxygen Species

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sulfoxide (-(S = O)-CH3 ), which can be further irreversibly oxidized to methionine sulfone (-(SO2 )-CH3 ). Methionine sulfoxide can be reduced by a large group of methionine sulfoxide reductases, which, along with target substrate specificity, exhibit stereoselectivity toward S- and R- isomers of methionine sulfoxide (125). As part of the catalytic cycle, methionine sulfoxide reductases utilize TRX as the electron donor; therefore, reduction of methionine sulfoxide is subject to limitations described in Section 3.1.2. Exposure of Arabidopsis to photorespiratory stress resulted in oxidation of methionine residues in approximately 400 proteins (59), indicating that methionine oxidation is a common PTM. However, compared with mechanisms involving cysteine oxidative PTMs, signaling events triggered by methionine oxidation remain largely uncharacterized. Most methionine oxidation events inactivate protein function (59, 79); however, recent data from bacterial models indicate that it might also have the opposite effect (38).


4. INTRACELLULAR INTERACTIONS BETWEEN ORGANELLE ROS AND REDOX SIGNALING It is common to compare gene expression data from chemical, genetic, and conditional alterations in ROS and redox homeostasis; however, the concept of a specific transcriptional marker gene is inaccurate (132). In a more recent cross-study comparison of microarrays, there did not seem to be direct correlation with the subcellular production site or ROS type, but rather with the temporal production of ROS and many later responses appeared to converge with the RBOHFmediated ROS burst (141). However, an outstanding question in ROS signaling is how signal origin information is retained or transmitted from the same ROS molecule produced in different subcellular compartments once the signal reaches the nucleus. This question is not likely to be answered by transcriptional analyses but rather from consideration of the biochemical nature and location of these molecules.

4.1. How Is Signaling Specificity Retained in the Cytosol? ROS alone are unable to transmit information about their site of origin. Initial predictions (96) therefore correctly suggested that (a) ROS might rely on site-specific sensors for signal perception, for which recently characterized and hypothetical mechanisms are described in Section 3, and that (b) signal specificity could be achieved through local production of secondary ROS messengers in the form of source-specific metabolites such as PAP (Sections 2.1.2 and 4.2), their oxidative derivatives, e.g., β-cyclocitral, or both (Section 2.1.1). Recent findings suggest that specificity could also be achieved by direct positioning of H2 O2 near the nuclear membrane from companion chloroplasts or stromule projections (Section 2.1.2). Other mechanisms might require the presence of diverse, spatially distinct internal receptors situated next to aquaporins within each compartment. The movement of ROS, e.g., through channels, could be sensed at the location of entry. Woo et al. (142) addressed this question using an animal system and demonstrated that activation of a plasma membrane receptor led to a decrease in local cytoplasmic ROS-scavenging, allowing the formation of local ROS maxima that might be sensed by proximal sensor proteins. This finding highlights the need to further characterize transporters or aquaporins in different compartment membranes in the context of ROS signal specificity (6). A seemingly analogous process is the regulation of Ca2+ stores, in which Ca2+ transport mechanisms involve diverse membrane- or compartment-specific transporters and internal or external sensing and activation mechanisms. For example, 10 calcineurin B-like Ca2+ sensor proteins (CBLs) and 26 CBL-interacting protein kinases (CIPKs) with cell type and subcellular spatial diversity have been identified in Arabidopsis (121), suggesting that they might contribute significantly to Ca2+ specificity. Although both ROS and Ca2+ molecules are tightly 222

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controlled to reduce damage, Ca2+ signatures are thought to confer specificity in the cytosol in the form of concentration fluctuations that are reproducibly distinct from particular stimuli. H2 O2 in contrast would not last long in the cytosol owing to scavenging, and compartment-specific location information would be rapidly lost owing to cytoplasmic streaming (96, 138).


4.2. Chloroplast-Mitochondrion Crosstalk, Signaling, and PAP As described in Section 2.1.2, the accumulation of PAP in chloroplasts has been suggested to act as a retrograde signal that relays information of chloroplastic redox state to the nucleus. However, there is evidence that this process involves additional interorganelle crosstalk. The specific series of events leading to activation of the PAP retrograde signal are as follows: 3 -phosphoadenosine5 -phosphosulfate (PAPS) is synthesized in the chloroplast and, to a lesser extent, in the cytoplasm. Following export from chloroplasts, PAPS is used in the cytoplasm as a sulfate donor for sulfotransferases (SOTs) such as SOT12 (9). The resulting PAP is transported back to the chloroplast via the PAPS/PAP antiporter PAPST1 according to a concentration gradient (9). Normally, the dual chloroplast-mitochondrion-localized PAP phosphatase, SAL1, then detoxifies PAP in chloroplasts and maybe also in mitochondria. However, changes in the chloroplastic redox state or in H2 O2 production can inactivate SAL1 (16), causing PAP accumulation. This correlates with the expression of specific nuclear genes, proposedly by affecting nuclear 5 -to-3 exoribonuclease activity. This promotes acclimation to high light, drought (16, 41), and plant immunity through regulation of SA- and JA-mediated signaling pathways (58). Although SAL1 is dual-targeted to both chloroplasts and mitochondria and is likely to be involved in mitochondrial retrograde signaling, it is at present only a putative sensor of mitochondrial redox status (135). The role and function of PAP in interorganellar signaling also appear increasingly complex by the likely involvement of the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1), originally identified as an O3 -induced lesion mutant (1). RCD1 is a nucleuslocalized transcriptional hub protein with a specific domain for protein-protein interactions (61, 105). RCD1 has been identified in multiple screens, including as one of five redox imbalance (rimb) mutants in a screen for mutants lacking chloroplastic redox-sensitive 2-Cys Prxr gene reporter activity, where it was suggested to be responsible for chloroplastic redox change–induced activation of antioxidant genes via interaction with the redox-regulated transcription factor RAP2.4a (54). A functional interaction between mitochondrial and chloroplastic retrograde signaling involving ANAC017 and PAP has been proposed (136). RCD1 has a role in mitochondrial ANAC013 and ANAC017 signaling (described in Section 2.1.2) owing to its direct interaction with ANAC013 (61, 105). ANAC017 is involved in the regulation of chloroplastic redox imbalance induced by methyl viologen (135), to which rcd1 is resistant (106). ANAC017 regulates the expression of ANAC013 (135), which, in addition to a self-amplifying loop, upregulates the MDS (28), and PAP induces the same genes (136). Because the rcd1 mutant has elevated expression of ANAC013 and other MDS genes (13, 61), RCD1 appears to be a negative regulator of PAP signaling and of the nuclear function of ANAC013. Although RCD1 may be involved in coordinating PAP-derived chloroplastic and mitochondrial redox states in the nucleus, how PAP retains specific information from organelles when it is synthesized in the cytosol is still unclear. A possible mechanism is through SOT12, which makes PAP from PAPS in the cytosol. Expression of SOT12 is negatively regulated by RCD1 (13, 61) and positively regulated by ANAC013 (28), ANAC017 (135, 136), and PAP (136), which suggests that the ROS- or redox-dependent inactivation of SAL1 in chloroplasts (16) will lead to an increase in cytoplasmic PAP concentration also by a positive feedback loop. This also implies either that a second organelle-specific signal is required for organelle specificity, or that chloroplastmitochondrion PAP responses are linked (102). www.annualreviews.org • Reactive Oxygen Species

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5. APOPLASTIC AND ORGANELLE ROS INTERACTIONS DURING STRESS As potent signaling molecules, ROS control many aspects of plant-environment interactions, as well as growth and development. In the following section we review major functions of ROS in long-distance signaling, plant-pathogen interactions, and stomatal closure.

5.1. Cell-to-Cell ROS Signaling Single-cell models do not adequately illustrate how ROS signals can affect the surrounding tissue and whole plant (Figure 4). A pivotal study by Miller et al. (94) identified a self-propagating


Apoplast

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Figure 4 ROS in long-distance signaling. Perception of local stimulus triggers rapid activation of NADPH oxidases that produce superoxide anions on the apoplastic side of the plasma membrane. Superoxide anions are dismutated to H2 O2 and diffuse within the apoplast to the neighboring cells. Apoplastic H2 O2 activates plasma membrane–located Ca2+ channels, ultimately leading to an increase in the concentration of Ca2+ in the cytoplasm resulting from an influx from the apoplast and other intracellular Ca2+ stores. Ca2+ activates RBOHD directly by binding to the EF-hands (Ca2+ -binding motifs) and indirectly by activating multiple CDPKs, which in turn results in accumulation of ROS within the apoplast of neighboring cells. These processes are most likely accompanied by signaling events triggered by apoplastic or cytoplasmic ROS sensors. Such a sequence of events allows the systemic spread of information in the form of a self-propelling wave. Abbreviations: CDPK, calcium-dependent protein kinase; ER, endoplasmic reticulum; GLR, glutamate receptor-like; RBOH, respiratory burst oxidase homolog; ROS, reactive oxygen species; TPC1, TWO-PORE CHANNEL1. 224

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mechanism for cell-to-cell signaling via RBOHD-derived apoplastic ROS—a central response to multiple internal ROS signaling mechanisms outlined above (141). The relatively oxidized state of the apoplast and low redox regulation and antioxidant capacity during stress would allow faster diffusion of H2 O2 in the apoplastic space than in the cytosol (49). Individual cell-to-cell ROS-relaying stations in the apoplast could also more rapidly diffuse signals than symplastic movement via plasmodesmata (138). Current gaps in these cell-to-cell models are (a) how do ROS signals in the apoplast reach and affect the cytosolic signaling components, (b) how do these initial compartment-specific ROS-sensing and ROS-signaling mechanisms retain specificity, and (c) how do they then relate to downstream hormone signaling. Since the discovery of the central role of RBOHD and the apoplastic movement of H2 O2 , more complex internal mechanisms for phosphorylation of NADPH oxidases have been elucidated in vivo in plants. Particularly important discoveries include MAMP and ROS-induced phosphorylation of RBOHD via the Ca2+ sensor CALCIUM-DEPENDENT PROTEIN KINASE5 (CPK5) (39); phosphorylation of RBOHD and RBOHF by CIPK26, CBL1, and CBL9 (122); and the discovery of the ROS-activated tonoplastic channel TWO-PORE CHANNEL 1 (TPC1), which releases Ca2+ into the cytosol during stress (24). This evidence suggests that coordination of Ca2+ and ROS signals occurs via Ca2+ -dependent phosphorylation of NADPH oxidases; however, other intersections such as the inclusion of vacuolar TPC1 in these models are still speculative (42, 122). In a similar way, long-distance electrochemical wound-activated surface potential changes require functional putative Ca2+ -permeable glutamate receptor-like cation channels, GLR3.3 and GLR3.6, which are activated cell autonomously almost immediately in the absence of a locally initiated ROS or Ca2+ wave (23, 99, 122). Given that GLR3.1 and GLR3.5 channels provide the basal cytoplasmic Ca2+ levels required to activate NADPH oxidases (75), it is tempting to speculate that this is also the case for GLR3.3 and GLR3.6. Electrochemical activation of GLR channels could also suggest analogous activation of specific electrochemically activated receptors required for opening aquaporins.

5.2. ROS in Plant Immunity and Stomatal Closure The phenomenon of enhanced disease resistance triggered by increased production of apoplastic ROS was demonstrated over 20 years ago. ROS have a direct antimicrobial effect; they are involved in cell wall stiffening and, most importantly, act as local and systemic signal molecules that are involved in the activation of antimicrobial defenses. 5.2.1. Regulation of apoplastic ROS sources and activity during plant-microbe interactions. With the use of specific inhibitors and mutant plants, multiple studies have contributed to our understanding of apoplastic ROS in plant immunity, and the role of NADPH oxidases (64, 73), apoplastic peroxidases (27), and PAOs (151, 152) is now established. However, it is difficult to determine the relative contributions of apoplastic ROS sources to the development of plant immune responses, because currently available data indicate that all three contribute to a successful defense. Their roles are most likely separated temporally, with activation of NADPH oxidases among the first processes following perception of MAMPs and apoplastic peroxidases and PAOs perhaps playing a role in later stages. Although multiple studies demonstrate partially overlapping functions of RBOHD and RBOHF, RBOHD appears to be a major isoform involved in plant immune responses. The predominant role of RBOHD can be observed at the level of promoter activity, as the RBOHD promoter is highly responsive to MAMP or pathogen treatments, whereas the RBOHF promoter is largely unresponsive (97). The primary role of RBOHD is also evident from the molecular www.annualreviews.org • Reactive Oxygen Species

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mechanisms following the perception of MAMPs by RLKs (64). In Arabidopsis, perception of MAMPs such as flagellin (epitope flg22) and elongation factor Tu (EF-Tu; epitopes elf18 and elf26) by their receptors leads to the activation of receptor-like cytoplasmic kinase BOTRYTISINDUCED KINASE1 (26), which further phosphorylates and activates RBOHD (65, 83). Signaling events leading to RBOH activation downstream of MAMP perception and those initiated by RLKs not directly involved in plant pathogen responses have been recently reviewed (26, 64, 73).

Chitosan: chitin-derived microbe-associated molecular pattern


Cytokinins: a group of plant hormones

5.2.2. Apoplast-to-chloroplast signaling. Among the most interesting events following the initial apoplastic ROS burst is the accumulation of ROS in the chloroplasts. The light dependency of the hypersensitive response suggests that chloroplasts have a crucial role in coordinating ROS production during plant immune responses (84). Similar conclusions can be drawn from a report demonstrating the negative influence of chloroplast 2-Cys Prxr on pathogen-induced cell death progression (57). Finally, multiple pathogen effectors target the chloroplastic electron transport chain to limit ROS production (30). However, it remains unknown how the apoplastic ROS burst is involved in the regulation of chloroplastic ROS production. Furthermore, whereas the function of chloroplastic ROS is established, it remains to be investigated how plants decrease their extensive chloroplast antioxidant capacity to allow ROS to accumulate. Results obtained by Nomura et al. (104) indicated that Ca2+ signaling mediated by chloroplastic CALCIUM SENSOR (CAS) is a major determinant of chloroplast function related to plant immunity. Recognition of MAMPs triggers plasma membrane Ca2+ influx channels to open, resulting in transient Ca2+ concentration fluctuations in the cytoplasm, followed by a prolonged CAS-dependent Ca2+ concentration increase in chloroplast stroma. Both early and late Ca2+ peaks were sensitive to inhibitors of serine/ threonine protein kinase and MAPKKs but were largely unaffected by an NADPH oxidase inhibitor. Further, cas plants exhibited partial reduction of late pathogen-induced ROS accumulation and impaired resistance to virulent and avirulent bacteria. Interestingly, CAS-dependent transcriptomic responses appear to significantly overlap with those triggered by the accumulation of 1 O2 (104), suggesting that 1 O2 has a role in executing a CAS-dependent pathogen-induced hypersensitive response. 5.2.3. ROS in the regulation of stomatal closure. Both RBOHD and RBOHF are necessary for executing stomatal closure in response to abscisic acid (ABA) and high levels of CO2 (19, 77). In contrast, stomatal movements initiated by perception of MAMPs rely mostly on RBOHD (85, 89). Successful activation of RBOH-mediated ROS production requires basal level of cytoplasmic Ca2+ , which is provided by the H2 O2 -independent plasma membrane GLUTAMATE RECEPTOR GLR3.1 and GLR3.5 Ca2+ influx channels (75). However, treatments with fungal elicitors such as yeast elicitor (71) and chitosan (72) or with cytokinins (2) rely mostly on apoplastic peroxidases as ROS sources. Furthermore, treatments with O3 (133) as well as H2 O2 (109) are sufficient to induce stomatal closure, indicating the existence of mechanisms for rapid perception of apoplastic ROS and execution of further signaling events required for stomatal closure. However, the actual perception mechanisms remain elusive (119). Recent data indicate that the entry of apoplastic ROS into the cytoplasm of guard cells is facilitated by aquaporin PIP2;1 as pip2;1 guard cells failed to accumulate H2 O2 in response to ABA and flg22 (115). Accumulation of ROS in the apoplast activates the still unidentified H2 O2 -dependent Ca2+ influx channels (107), and the increase in cytoplasmic Ca2+ concentration triggers secondary Ca2+ transients in chloroplasts as well as activation of multiple Ca2+ -dependent protein kinases that further stimulate the activity of RBOHs and activate anion channels (119). At the same time, ROS accumulation in the guard cell chloroplasts is increased (133).

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Most signaling pathways leading to stomatal closure involve the function of OPEN STOMATA1 (OST1), which serves as a hub of information flow (119). The only stimulus identified thus far that triggers stomatal closure in ost1 mutant plants is PAP (108), indicating that the activity of CPKs is sufficient to execute stomatal closure. This recent finding agrees with a previous report demonstrating reduced stomatal response to abscisic acid in the cpk5 cpk6 cpk11 cpk23 quadruple mutant despite intact OST1 function (12). Thus, it was hypothesized that OST1 might act primarily upstream of apoplastic ROS production and that part of the phenotypes observed in ost1 mutants could be related to impaired activation of the ROS-regulated Ca2+ channels and consequential compromised activation of CPKs (119). Further, the activity of OST1 is negatively regulated by protein phosphatases type 2C, some of which in turn are inhibited by H2 O2 (88), suggesting the existence of a self-amplifying loop linking OST1 and H2 O2 in stomatal closure.

Casparian strip: a structure located within the root endodermis that prevents free passage of solutes

6. ROS IN PLANT DEVELOPMENT As evident from the previous sections, ROS are crucial regulators of metabolism and plant stress responses. However, in addition to these canonical functions, ROS are also inherent to multiple processes regulating plant development. In this context, most of the available functional data establish apoplastic ROS as the primary regulator of these processes. Here, we review selected developmental processes that require active ROS production. Well-characterized developmental processes involving apoplastic ROS production are pollen tube formation and root hair growth. RBOHC is the primary ROS-producing enzyme required for the root hair elongation, as rbohC mutants are deficient in this process (47). RBOHC exhibits polar subcellular localization associated mainly with the tip apex. Stimulation of apoplastic ROS production triggers an influx of extracellular Ca2+ , which is required for cell elongation. Analogous to RBOH regulation in guard cell signaling, an influx of Ca2+ further activates RBOHC, creating a positive feedback loop (124). Following these initial discoveries, Jones et al. (63) found that production of O2 ·− at the root hair tip depended on RHO-RELATED PROTEIN FROM PLANTS2, a GTPase acting upstream of RBOHC controlling ROS production. Conceptually similar sequences of events control the polarized pollen tube elongation. Two apparently redundant RBOH isoforms, RBOHH and RBOHJ, served as sources of apoplastic ROS and were crucial for proper pollen tube growth (10, 69, 78). Although the precise mechanisms regulating RBOHH and RBOHJ activity remain to be elucidated, two Catharanthus roseus RLK1-like (CrRLK1L) family kinases, ANXUR1 and ANXUR2, appear to be involved in this process, as anx1 anx2 double mutants exhibited pollen tube growth deficiency and phenotypes observed in ANXUR1 overexpressors were dependent on functional RBOHH and RBOHJ (10). In addition to establishing the primary cell wall structure, apoplastic ROS are instrumental in regulating the development of secondary cell wall architecture. Cell wall lignification is among the secondary events following the perception of cell wall damage (CWD), and ROS produced by RBOHD are necessary for the execution of this response (52). Mutants deficient in RBOHD exhibit reduced lignin deposition and this effect is further intensified in the rbohD rbohF double mutant (34). In the context of CWD signaling, the activity of RBOHD and RBOHF appears to be controlled by the THESEUS1 CrRLK1L kinase, as the1 mutants accumulated less apoplastic ROS following the induction of CWD (34). In contrast to lignification induced by CWD, the developmentally regulated formation of the Casparian strip within the endodermis relies solely on the function of RBOHF (80). Interestingly, this production of precisely localized ROS appears to be determined by recruitment of RBOHF to the site of lignin deposition by Casparian strip domain proteins as well as specific activation of RBOHF activity, as rbohF plants expressing the RBOHF catalytic domain under the control of the www.annualreviews.org • Reactive Oxygen Species

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RBOHB regulatory domain failed to develop the Casparian strip (80). This observation implies the existence of a specific mechanism for regulating RBOHF activity that is not yet understood.

7. CONCLUSIONS


ROS are ubiquitous metabolites in all aerobic organisms and were originally regarded only as unwanted substances damaging to cells. However, studies performed over the course of the past two decades and earlier have elucidated cellular and molecular mechanisms involved in the adaptation and acclimation of plants to their environment, highlighting the important signaling function for ROS in these processes, and the concept of ROS as signaling substances has been established. Now, it is clearly recognized that controlled production of ROS enables these critical signals to act in response to stress and in development. This implies that there must be coordinated function of signaling networks that govern ROS-responses, although detailed descriptions of how such interactions work are still mostly lacking. Furthermore, the perception of ROS and the immediate processes downstream of perception are still almost completely unknown in any species. Studies addressing these questions will result in discoveries of new, previously uncharacterized ROSrelated regulatory mechanisms involved in the coordination of plant gene expression as well as in the adaptation and acclimation of plants to their surrounding conditions. SUMMARY POINTS 1. ROS levels are tightly controlled; increased ROS production rates do not necessarily translate into elevated steady-state concentrations of ROS. 2. Increased ROS production or levels often serve as initiation signals for multiple signaling pathways. 3. Plants respond to ROS in a ROS molecule type- and localization-dependent manner. 4. ROS signaling specificity is likely determined by local ROS sensors and the production of metabolites, their derivatives, or both. 5. The accumulation of ROS is necessary for multiple metabolic, physiological, and developmental processes that function at the cellular and whole-organism levels.

FUTURE ISSUES 1. Multiple ROS-sensing mechanisms have been recently documented or suggested. However, although indirect evidence suggests their existence, some mechanisms, e.g., sensing of apoplastic ROS, remain unidentified. 2. In many cases, ROS accumulation is connected with Ca2+ signals. However, it is not clear how these stimuli are connected. In this context, the most outstanding questions relate to the identity of Ca2+ channels and their activation mechanisms. 3. Multiple lines of evidence support the concept of locality in ROS signaling. Therefore, special emphasis should be dedicated to the spatial distribution of potential ROS sensors. In this context, the use of up-to-date tools for monitoring local ROS maxima should provide better information than approaches in which the whole leaf or whole cell is analyzed.

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4. Recent documentation of chloroplast-to-nucleus protein and H2 O2 transport means that the previously proposed retrograde signaling pathways based on ROS diffusion to the cytoplasm should be reevaluated, given that cytoplasmic ROS can arise from multiple sources. 5. Although the signaling function of metabolites and their oxidative derivatives begins to emerge, there are probably many more such signaling molecules that await identification.


6. The relationship between compartment-specific perturbations in redox balance and ROS formation, and how they affect each other, is not always clear and will need to be addressed to determine exactly how they contribute to different signaling pathways.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We thank Estee Tee and Kai Xun Chan from the Pogson laboratory, and Ian Max Møller for useful comments and discussions during the preparation of the manuscript. All authors are members of the Centre of Excellence in the Molecular Biology of Primary Producers (2014–2019). C.W. is funded by the Academy of Finland (decision #294580). LITERATURE CITED 1. Ahlfors R, La˚ng S, Overmyer K, Jaspers P, Brosché M, et al. 2004. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–37 2. Arnaud D, Lee S, Takebayashi Y, Choi D, Choi J, et al. 2017. Cytokinin-mediated regulation of reactive oxygen species homeostasis modulates stomatal immunity in Arabidopsis. Plant Cell 29:543–59 3. Asada K. 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141:391–96 4. Attacha S, Solbach D, Bela K, Moseler A, Wagner S, et al. 2017. Glutathione peroxidase-like enzymes cover five distinct cell compartments and membrane surfaces in Arabidopsis thaliana. Plant Cell Environ. 40:1281–95 5. Awad J, Stotz HU, Fekete A, Krischke M, Engert C, et al. 2015. 2-Cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water-water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions. Plant Physiol. 167:1592–603 6. Bienert GP, Chaumont F. 2014. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta 1840:1596–604 7. Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, et al. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47:851–63 8. Bleier L, Drose ¨ S. 2013. Superoxide generation by complex III: from mechanistic rationales to functional consequences. Biochim. Biophys. Acta 1827:1320–31 9. Bohrer A-S, Kopriva S, Takahashi H. 2015. Plastid-cytosol partitioning and integration of metabolic pathways for APS/PAPS biosynthesis in Arabidopsis thaliana. Front. Plant Sci. 5:751 10. Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U. 2013. ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLOS Biol. 11:e1001719 www.annualreviews.org • Reactive Oxygen Species

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39. Demonstrated MAMP- and ROS-induced phosphorylation of RBOHD via the Ca2+ sensor CPK5.

43. Identified a novel retrograde mechanism for direct nuclear transport of H2 O2 from chloroplasts in close proximity to nuclei.

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65. Demonstrated direct activation of the NADPH oxidase RBOHD by the protein kinase BIK1.

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78. Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T. 2014. Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J. 78:94–106 79. Lee S-H, Li C-W, Koh KW, Chuang H-Y, Chen Y-R, et al. 2014. MSRB7 reverses oxidation of GSTF2/3 to confer tolerance of Arabidopsis thaliana to oxidative stress. J. Exp. Bot. 65:5049–62 80. Lee Y, Rubio MC, Alassimone J, Geldner N. 2013. A mechanism for localized lignin deposition in the endodermis. Cell 153:402–12 81. Leister D. 2017. Piecing the puzzle together: the central role of ROS and redox hubs in chloroplast retrograde signaling. Antioxid. Redox Signal. In press. https://doi.org/10.1089/ars.2017.7392 82. Li J, Liu J, Wang G, Cha J-Y, Li G, et al. 2015. A chaperone function of NO CATALASE ACTIVITY1 is required to maintain catalase activity and for multiple stress responses in Arabidopsis. Plant Cell 27:908–25 83. Li L, Li M, Yu L, Zhou Z, Liang X, et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe. 15:329–38 84. Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. 2007. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J. 51:941–54 85. Macho AP, Boutrot F, Rathjen JP, Zipfel C. 2012. Aspartate oxidase plays an important role in Arabidopsis stomatal immunity. Plant Physiol. 159:1845–56 86. Martinez C, Montillet JL, Bresson E, Agnel JP, Dai GH, et al. 1998. Apoplastic peroxidase generates superoxide anions in cells of cotton cotyledons undergoing the hypersensitive reaction to Xanthomonas campestris pv. malvacearum Race 18. Mol. Plant-Microbe Interact. 11:1038–47 87. Mattila H, Khorobrykh S, Havurinne V, Tyystjärvi E. 2015. Reactive oxygen species: reactions and detection from photosynthetic tissues. J. Photochem. Photobiol. 152:176–214 88. Meinhard M, Rodriguez PL, Grill E. 2002. The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214:775–82 89. Mersmann S, Bourdais G, Rietz S, Robatzek S. 2010. Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol. 154:391–400 90. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, et al. 2007. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 52:973–86 91. Meyer Y, Belin C, Delorme-Hinoux V, Reichheld J-P, Riondet C. 2012. Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid. Redox Signal. 17:1124–60 92. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G. 2010. Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J. Exp. Bot. 61:4197–220 93. Miao Y, Lv D, Wang P, Wang X-C, Chen J, et al. 2006. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–66 94. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, et al. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45 95. Mishina NM, Tyurin-Kuzmin PA, Markvicheva KN, Vorotnikov AV, Tkachuk VA, et al. 2011. Does cellular hydrogen peroxide diffuse or act locally? Antioxid. Redox Signal. 14:1–7 96. Møller IM, Sweetlove LJ. 2010. ROS signalling–specificity is required. Trends Plant Sci. 15:370–74 97. Morales J, Kadota Y, Zipfel C, Molina A, Torres M-A. 2016. The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. J. Exp. Bot. 67:1663–76 98. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, et al. 2008. Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2 O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–24 99. Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. GLUTAMATE RECEPTORLIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422–26 www.annualreviews.org • Reactive Oxygen Species

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Annual Review of Plant Biology

Contents

Volume 69, 2018


My Secret Life Mary-Dell Chilton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Diversity of Chlorophototrophic Bacteria Revealed in the Omics Era Vera Thiel, Marcus Tank, and Donald A. Bryant p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21 Genomics-Informed Insights into Endosymbiotic Organelle Evolution in Photosynthetic Eukaryotes Eva C.M. Nowack and Andreas P.M. Weber p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p51 Nitrate Transport, Signaling, and Use Efficiency Ya-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay p p p p p p p p p p p p p p p p p p p p p85 Plant Vacuoles Tomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa, and Ikuko Hara-Nishimura p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 123 Protein Quality Control in the Endoplasmic Reticulum of Plants Richard Strasser p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 147 Autophagy: The Master of Bulk and Selective Recycling Richard S. Marshall and Richard D. Vierstra p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 173 Reactive Oxygen Species in Plant Signaling Cezary Waszczak, Melanie Carmody, and Jaakko Kangasjärvi p p p p p p p p p p p p p p p p p p p p p p p p p p 209 Cell and Developmental Biology of Plant Mitogen-Activated Protein Kinases ˇ ˇ George Komis, Olga Samajov´ a, Miroslav Oveˇcka, and Jozef Samaj p p p p p p p p p p p p p p p p p p p p p 237 Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling Xiangxiu Liang and Jian-Min Zhou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267 Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity to Immunity and Beyond Christina Maria Franck, Jens Westermann, and Aurélien Boisson-Dernier p p p p p p p p p p p p 301 Kinesins and Myosins: Molecular Motors that Coordinate Cellular Functions in Plants Andreas Nebenfuhr ¨ and Ram Dixit p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 329 v

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The Oxylipin Pathways: Biochemistry and Function Claus Wasternack and Ivo Feussner p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 363 Modularity in Jasmonate Signaling for Multistress Resilience Gregg A. Howe, Ian T. Major, and Abraham J. Koo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 387 Essential Roles of Local Auxin Biosynthesis in Plant Development and in Adaptation to Environmental Changes Yunde Zhao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 417 Genetic Regulation of Shoot Architecture Bing Wang, Steven M. Smith, and Jiayang Li p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 437 Annu. Rev. Plant Biol. 2018.69:209-236. Downloaded from www.annualreviews.org Access provided by Helsinki University on 05/28/18. For personal use only.

Heterogeneity and Robustness in Plant Morphogenesis: From Cells to Organs Lilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa, Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder p p p p p p 469 Genetically Encoded Biosensors in Plants: Pathways to Discovery Ankit Walia, Rainer Waadt, and Alexander M. Jones p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 497 Exploring the Spatiotemporal Organization of Membrane Proteins in Living Plant Cells Li Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin p p p p p p p p p p p p p p p p p p p p p p p 525 One Hundred Ways to Invent the Sexes: Theoretical and Observed Paths to Dioecy in Plants Isabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai p p p p p p p p p p p p p p p p p p p p p p 553 Meiotic Recombination: Mixing It Up in Plants Yingxiang Wang and Gregory P. Copenhaver p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 577 Population Genomics of Herbicide Resistance: Adaptation via Evolutionary Rescue Julia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright p p p p p p p p p p p p p p p p p p p p p p p p p 611 Strategies for Enhanced Crop Resistance to Insect Pests Angela E. Douglas p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 637 Preadaptation and Naturalization of Nonnative Species: Darwin’s Two Fundamental Insights into Species Invasion Marc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi, and Nicholas E. Mandrak p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 661 Macroevolutionary Patterns of Flowering Plant Speciation and Extinction Jana C. Vamosi, Susana Magallón, Itay Mayrose, Sarah P. Otto, and Hervé Sauquet p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 685

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When Two Rights Make a Wrong: The Evolutionary Genetics of Plant Hybrid Incompatibilities Lila Fishman and Andrea L. Sweigart p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 707 The Physiological Basis of Drought Tolerance in Crop Plants: A Scenario-Dependent Probabilistic Approach Fran¸cois Tardieu, Thierry Simonneau, and Bertrand Muller p p p p p p p p p p p p p p p p p p p p p p p p p p p p 733


Paleobotany and Global Change: Important Lessons for Species to Biomes from Vegetation Responses to Past Global Change Jennifer C. McElwain p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 761 Trends in Global Agricultural Land Use: Implications for Environmental Health and Food Security Navin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis, Claire Kremen, Mario Herrero, and Loren H. Rieseberg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 789 Errata An online log of corrections to Annual Review of Plant Biology articles may be found at http://www.annualreviews.org/errata/arplant

Contents

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