How Extracellular Reactive Oxygen Species Reach Their Intracellular Targets in Plants

Jinsu Lee, Minsoo Han, Yesol Shin, Jung-Min Lee, Geon Heo

Abstract

Reactive oxygen species (ROS) serve as secondary messengers that regulate various developmental and signal transduction processes, with ROS primarily generated by NADPH OXIDASEs (referred to as RESPIRATORY BURST OXIDASE HOMOLOGs [RBOHs] in plants). However, the types and locations of ROS produced by RBOHs are different from those expected to mediate intracellular signaling. RBOHs produce O₂^•− rather than H₂O₂ which is relatively long-lived and able to diffuse through membranes, and this production occurs outside the cell instead of in the cytoplasm, where signaling cascades occur. A widely accepted model explaining this discrepancy proposes that RBOH-produced extracellular O₂^•− is converted to H₂O₂ by superoxide dismutase and then imported by aquaporins to reach its cytoplasmic targets. However, this model does not explain how the specificity of ROS targeting is ensured while minimizing unnecessary damage during the bulk translocation of extracellular ROS (eROS). An increasing number of studies have provided clues about eROS action mechanisms, revealing various mechanisms for eROS perception in the apoplast, crosstalk between eROS and reactive nitrogen species, and the contribution of intracellular organelles to cytoplasmic ROS bursts. In this review, we summarize these recent advances, highlight the mechanisms underlying eROS action, and provide an overview of the routes by which eROS-induced changes reach the intracellular space.

Keywords: NADPH oxidase, peroxidase, reactive oxygen species, receptor-like kinase, superoxide dismutase

INTRODUCTION

Reactive oxygen species (ROS) are inevitable by-products of photosynthesis and metabolic processes in plants. In addition, ROS are actively produced and used as signaling molecules in various developmental processes and in biotic and abiotic stress responses (Huang et al., 2019; Mittler et al., 2022; Waszczak et al., 2018). Along with calcium and electrical signals, ROS also form waves that act as systemic signals that are rapidly propagated and trigger stress responses in tissues throughout the plant (Choi et al., 2017; Fichman and Mittler, 2020; Fichman et al., 2019). The most widely investigated mechanism of redox status-mediated signaling involves post-translational modifications of target proteins through the oxidation of methionine to sulfoxide and of cysteine to sulfenic, sulfinic, and sulfonic acids (Petushkova and Zamyatnin, 2020). Since ROS can also cause irreversible oxidative damage to DNA, lipids, and proteins, sophisticated spatiotemporal regulatory mechanisms for ROS metabolism are employed to effectively detoxify ROS produced by multiple mechanisms while specifically activating signaling pathways at the appropriate locations and times.

ROS is a collective term for a number of reactive molecules derived from molecular oxygen, including singlet oxygen (¹O₂), superoxide radical anion (O₂^•−), and other oxygen radicals as well as non-radical derivatives of O₂ such as hydrogen peroxide (H₂O₂) and hypochlorous acid (HOCl). These molecules exhibit diverse spectra of reactivity, half-life, diffusion, and potential to generate additional downstream reactive species (Möller et al., 2019; Murphy et al., 2022). H₂O₂, which has a relatively long lifetime and low reactivity, is highly soluble in both lipid and aqueous environments, allowing it to freely diffuse through cell membranes to distances of up to several cell diameters before reacting with specific targets (Scheel and Wasternack, 2002). Because of these properties, H₂O₂ is regarded as the principal ROS used in signaling. Notably, however, NADPH oxidase (also called respiratory burst oxidase homolog [RBOH] in plants), which is the major enzyme that generates ROS for signal transduction in a wide range of cellular processes, generates O₂^•−, not H₂O₂, and does so outside the cell rather than inside (Kumar et al., 2007; Torres et al., 2002). These observations suggest that the activities of various antioxidant enzymes are coordinated to fine-tune ROS concentrations as well as the types and distribution of ROS.

O₂^•− is a precursor to H₂O₂, but it performs distinct biological functions (Chen et al., 2022; Lee et al., 2018; Tsukagoshi et al., 2010; Zeng et al., 2017). O₂^•− itself can be transported across cell membranes, and the channels responsible for this have been identified in animals (Fisher, 2009; Hawkins et al., 2007). O₂^•− and H₂O₂ show different distribution patterns in Arabidopsis (Arabidopsis thaliana) roots, with O₂^•− mainly occurring in the meristematic zone of the root tip and H₂O₂ in the elongation zone; the balance of these two ROS influences the cellular transition from proliferation to differentiation (Dunand et al., 2007; Tsukagoshi et al., 2010; Yamada et al., 2020). Cell type-specific ROS distribution is also essential for stem cell maintenance in shoot apical meristems and for floral organ abscission (Lee et al., 2018; Zeng et al., 2017). Thus, growing evidence suggests that the concentrations and types of ROS are finely regulated to mediate various cellular processes. In this review, we take a closer look at these processes to provide insight into how the spatiotemporal balance of ROS is maintained, how the specificity of ROS action is ensured, and how extracellular ROS (eROS) reach their signaling targets inside cells.

ACCUMULATION OF eROS FOR SIGNAL TRANSDUCTION: SYNTHESIS AND DETOXIFICATION

Since ROS are continuously generated as by-products of metabolic processes, cells have various enzymatic and non-enzymatic systems to detoxify these molecules (Mittler, 2002). Therefore, raising the ROS concentration to a specific threshold required for signal transduction involves both the activation of ROS-generating enzymes and the local inactivation of detoxifying enzymes.

In Arabidopsis, RBOHs are encoded by 10 homologous genes, RBOHA to RBOHJ (Doke, 1985; Mittler et al., 2011). These enzymes function in a wide range of cellular processes such as guard cell movement, root hair growth, senescence, wound healing, and defense responses (Koo et al., 2017; Kumar et al., 2007; Miller et al., 2009; Torres et al., 2002). The role of RBOH-generated ROS in signaling pathways is conserved in many plants, including rice (Oryza sativa), maize (Zea mays), and tomato (Solanum lycopersicum) (Nestler et al., 2014; Sagi et al., 2004; Yoshie et al., 2005). In addition to RBOHs, peroxidases and polyamine oxidases also contribute to eROS generation (Do et al., 2019; Kaman-Toth et al., 2019; Yu et al., 2019), suggesting that ROS levels are regulated via sophisticated multi-layered mechanisms.

The activity of RBOHs is controlled by multiple post-translational modifications including phosphorylation, Ca²⁺ binding, nitrosylation, persulfidation, and ubiquitination (Chen et al., 2017; Dubiella et al., 2013; Lee et al., 2020; Ogasawara et al., 2008; Shen et al., 2020; Sirichandra et al., 2009; Yun et al., 2011). Phosphorylation by Ca²⁺-regulated protein kinases and Ca²⁺ binding to EF-hand motifs are the most ubiquitous mechanisms for regulating RBOH activity (Dubiella et al., 2013; Kobayashi et al., 2007; Ogasawara et al., 2008). The physiological roles of these and other post-translational modifications in the multilayered regulation of RBOH activity are gradually being revealed. For example, during the plant immune response, the central immune kinase BOTRYTIS-INDUCED KINASE 1 (BIK1) phosphorylates RBOHD independently of Ca²⁺, and yet this process is essential for Ca²⁺-based regulation of RBOHD (Kadota et al., 2014; Li et al., 2014). This two-step regulatory process ensures the specificity of immune-associated ROS bursts even though Ca²⁺-based regulation mediates diverse responses. By contrast, serine-threonine protein phosphatases inhibit RBOH activity. The SnRK2-type kinase OPEN STOMATA1 (OST1) is activated by abscisic acid (ABA), leading to the phosphorylation of RBOHF and subsequently stomatal closure. In the absence of ABA, dephosphorylation by PP2CA, a type 2C protein phosphatase (PP2C) family protein, inhibits OST1 activity and RBOHF-mediated stomatal closure (Brandt et al., 2012; Lee et al., 2009; Sirichandra et al., 2009). The activity of RBOHD is also controlled by persulfidation (Shen et al., 2020) during ABA signaling in guard cells. Interestingly, ROS react with this modification to form perthiosulfenic acid, thereby returning RBOHD activity to its basal state, suggesting that ROS generated by RBOH can act as a negative feedback signal to control the duration of RBOH activation.

A widely accepted model posits that the O₂^•− produced by RBOH is converted to H₂O₂ by SUPEROXIDE DISMUTASE (SOD) before migrating into the cytoplasm via aquaporins (Apel and Hirt, 2004; Bienert et al., 2007). While the identity and regulatory mechanisms of extracellular SODs (eSODs) have been well described in animals (Fattman et al., 2003), there is only limited information on eSODs involved in ROS-mediated signaling in plants. An SOD is classified as either Cu Zn SOD (CSD), Mn SOD (MSD) or Fe SOD (FSD), depending on its metal coenzyme(s) (Alscher et al., 2002). Eight genes encode SODs in the Arabidopsis genome: CSD1–3, MSD1 and 2, and FSD1–3 (Chen et al., 2022; Miller, 2012). Among the products encoded by these genes, MSD2 is the only one that is secreted out of the cell (Chen et al., 2022; Lee et al., 2022). MSD2 shows SOD activity at a broad range of pH levels and is strongly expressed in specific cell types, such as those in the root tips and abscission zones, suggesting that ROS metabolism regulated by MSD2 is linked to specific signaling pathways. Indeed, phenotypic analysis of msd2 mutants revealed that MSD2 regulates root morphogenesis during light-to-dark transitions (Chen et al., 2022) as well as floral organ abscission (Lee et al., 2022), demonstrating its participation in ROS-mediated signaling pathways.

H₂O₂ is broken down into water and oxygen by catalases (CATs) or peroxidases (PRXs) (Apel and Hirt, 2004). PRXs are divided into three classes: Class I, II, and III. Class III PRXs are secreted into the vacuole and apoplast (Andrews et al., 2002; Takabe et al., 2001) and are involved in various physiological processes, such as cell wall metabolism, seed germination, wound healing, and defense against pathogens (Movahed et al., 2016; Passardi et al., 2004b; Shigeto and Tsutsumi, 2016). PRXs not only break down ROS but also generate H₂O₂, as is done by PRX33 and PRX34 in response to pathogen attack (Kaman-Toth et al., 2019; Zhao et al., 2019) and by PRX62 and PRX69 to regulate root hair growth under low-temperature conditions (Pacheco et al., 2022). Since the ROS substrates and products of PRX also play important roles in signal transduction, understanding how these two opposing activities of PRX are regulated is a remaining task. CATs are also involved in maintaining ROS homeostasis. The expression of CAT2 during stomatal development is directly regulated by SPEECHLESS, the master regulator of stomatal development, which regulates cell type-specific ROS patterns (Shi et al., 2022). As extracellular catalase has been reported in animals (Bohm et al., 2015) but not yet in plants, it remains a question whether this action of catalase can also occur extracellularly.

MULTIFACETED ROUTS FOR eROS TO REACH INTRACELLULAR SIGNALING COMPONENTS

Perception of eROS outside the cell

The apoplast, where the concentrations of antioxidants and ROS are relatively low (Zechmann and Müller, 2010), would be an ideal site to quickly reach the ROS levels required for signal transduction while minimizing damage to surrounding proteins. The advantages of eROS can be maximized when the targets are also extracellular. Indeed, recent studies have demonstrated that receptors capable of recognizing eROS and initiating signal transduction exist outside the cell.

For instance, the plasma membrane contains numerous receptor-like kinases (RLKs) with ectodomains that can detect molecular changes in the apoplast, possibly including eROS (Morillo and Tax, 2006; Wrzaczek et al., 2010). HPCA1 (HYDROGEN-PEROXIDE-INDUCED Ca²⁺ INCREASES 1), an LRR-RK (leucine rich repeat-receptor kinase), was recently identified as a crucial regulator of eH₂O₂-induced increases in Ca²⁺ levels in Arabidopsis (Wu et al., 2020). Cysteine residues in the HPCA1 ectodomain are directly modified by eH₂O₂, which induces the autophosphorylation and activation of Ca²⁺ channel proteins, revealing that HPCA1 is an eH₂O₂ sensor. HPCA1 acts as a key eROS receptor during plant adaptation to various biotic and abiotic stresses, systemic signaling, and cell-to-cell ROS signal propagation (Fichman et al., 2022; Laohavisit et al., 2020).

Ion channels in the plasma membrane could also act as sensors of eROS. The ability of ROS to activate ion conduction in plant membranes has long been known in relation to Cu²⁺ toxicity in the charophyte alga Nitella flexilis (Demidchik et al., 1997; 2001). Indeed, a variety of ion channels have been shown to be activated by ROS in Arabidopsis, Asian pear (Pyrus pyrifolia), pea (Pisum sativum), and Lilium longiflorum, including inwardly and outwardly rectifying channels and voltage-independent channels that function in tip growth and plant responses to various stresses (Demidchik, 2018). Garcia-Mata et al. (2010) provided clues about the molecular mechanism underlying ROS-induced activation of the STELAR K⁺ outward rectifier (SKOR) in Arabidopsis. Using heterologous expression systems in HEK293 cells and Xenopus oocytes, the authors demonstrated that the Cys¹⁶⁸ residue in the S3 α-helix within the voltage sensor of the channel of SKOR is essential for its sensitivity to H₂O₂. The water-filled pocket in which Cys¹⁶⁸ is located is large enough to accept H₂O₂ and is exposed to the external bulk solution upon depolarization, suggesting that this site is a target of eROS. The corresponding Cys residue is also conserved in the GORK (gated outwardly rectifying K⁺ channel), suggesting that additional channels with ROS-sensing cysteine moieties remain to be discovered.

eROS-mediated cell wall modification

Considering that the ectodomains of membrane proteins can be modified by eROS, the cell wall and cell wall proteins might also be influenced by eROS. Indeed, the effects of ROS on cell wall loosening have been reported (Airianah et al., 2016; Fry, 1998; Müller et al., 2009). ROS, especially hydroxyl radicals (OH^•), can cleave cell wall polymers such as xyloglucan and pectin, thereby promoting cell elongation. Conversely, the accumulation of H₂O₂ causes the cross-linking of cell wall components and restricts elongation, making it difficult to pinpoint the role of eROS in the cell wall.

Cell wall modification by eROS is often mediated by class III PRXs. Class III PRXs are encoded by large multigene families (75 genes in Arabidopsis and 138 genes in rice) (Passardi et al., 2004a; Valerio et al., 2004) and catalyze the oxidation of numerous substrates such as extensins, monolignols, ferulic acids, and suberin using H₂O₂ as the electron acceptor (Lee et al., 2013; Shigeto and Tsutsumi, 2016). Class III PRX reactions have different effects, depending on the substrate. In vitro experiments with maize coleoptiles showed that H₂O₂ promotes cell wall stiffening and that this effect is maintained during indole-3-acetic acid (IAA)- and acid-mediated growth (Schopfer, 1996). The wall-stiffening reaction in maize coleoptiles triggered by H₂O₂ is mediated by PRX, which induces phenolic cross-linking in the cell wall. Potential phenolic substrates for PRX-catalyzed oxidative cross-linking include lignin precursors, tyrosine residues of certain glycoproteins, and ester-linked hydroxycinnamic-acid residues of pectic or hemicellulosic polysaccharides (Francoz et al., 2015; Passardi et al., 2004b).

Changes in the cell wall can be perceived by plasma membrane-localized RLKs and mechanosensitive ion channels, which initiate intracellular signaling cascades (Basu and Haswell, 2020; Radin et al., 2021; Vaahtera et al., 2019). THESEUS1/FERONIA family RLKs in Arabidopsis can potentially sense changes in cell wall integrity to modulate downstream cell signaling pathways (Bacete et al., 2022; Feng et al., 2018; Lin et al., 2022). Depending on the concentration and longevity of eROS, their effects on cell wall integrity are highly variable. How sensitive the cell wall is to eROS, to what extent cell wall integrity receptors detect changes in the cell wall, and how specificity can be ensured during various interactions with eROS remain to be determined.

Crosstalk between eROS and nitric oxide signaling

Reactive nitrogen species (RNS), along with ROS, act as important signaling molecules in plants and regulate a variety of processes including development, growth, and responses to abiotic and biotic stress (Domingos et al., 2015; Turkan, 2017). RNS induce post-translational modifications, such as S-nitrosylation and tyrosine nitration, causing conformational changes that affect the activity and localization of target proteins.

Nitric oxide (NO^•), a highly reactive small gaseous molecule, modulates the expression of several genes involved in hormonal signaling, primary metabolism, and stress responses (Palmieri et al., 2008; Safavi-Rizi et al., 2020). In addition to cytosolic NO^•, various physiological functions of apoplastic NO^• have been reported (Besson-Bard et al., 2008; Bethke et al., 2004; StoÈhr and Ullrich, 2002). The root-specific membrane-bound nitrite reductase (Ni:NOR) and NR (nitrate reductase) are thought to be responsible for apoplastic RNS generation, which is important for root growth, symbiotic interactions, and drought tolerance (Silveira et al., 2017; Stöhr and Stremlau, 2006).

The bioavailability and action of NO^• are modulated by its reaction with O₂^•− to generate a more reactive peroxide, peroxynitrite (ONOO−), which possesses characteristics of both O₂^•− reactivity and NO^• mobility and functions as a signaling molecule. SOD3, an eSOD in animal cells, is thought to regulate ONOO− availability by controlling NO^•/O₂^•− reactions, which in turn stabilizes the transcription factor HIF-2α to improve tumor-responsive gene expression (Carmona-Rodríguez et al., 2020; Mira et al., 2018). eSOD and RNS were recently shown to interact in floral organs of Arabidopsis during abscission. ONOO− promotes abscission by regulating the expression levels of major signaling components, and MSD2, an eSOD, is involved in this regulation (Lee et al., 2022). Interacting with NO^• could represent a major role for O₂^•− distinct from that of H₂O₂ in plants, and eSOD could regulate the balance between ROS and RNS.

Coordination with organellar ROS generation

Cytosolic ROS bursts are observed under various biotic and abiotic stress conditions. Although eROS produced by RBOH are considered to be the direct sources of cytoplasmic ROS bursts, it is difficult to prove how many eROS are actually imported into the cell. It cannot be discounted that intracellular organelles such as mitochondria, chloroplasts, and peroxisomes, where large amounts of ROS are produced, contribute to the generation of cytosolic ROS (Del Río and López-Huertas, 2016; Mubarakshina et al., 2010; Zorov et al., 2006).

Intracellular ROS accumulation is important for ABA-induced stomatal closure, which is mediated by RBOHD and RBOHF (Kwak et al., 2003). Contrary to the long-standing model of eROS transport, recent reports have focused on ROS released from the chloroplast (Iwai et al., 2019). Indeed, ABA-induced ROS are first observed in chloroplasts, and cytosolic ROS bursts can be eliminated by inhibiting photosynthetic electron transport (PET). These observations suggest that PET-mediated ROS contribute to ROS bursts that influence ABA‐induced stomatal closure. A similar contribution of chloroplastic ROS has been reported to regulate the hypersensitive response in tobacco (Liu et al., 2007). Thus, intracellular organelles may commonly contribute to ROS signaling.

PERSPECTIVES

Accumulating evidence points to the involvement of ROS in various signaling and developmental processes, but our understanding of the regulatory mechanisms underlying ROS generation, conversion, and degradation as well as the roles of these molecules as messengers is fragmentary. In this review, we provided a perspective on the various routes of eROS-mediated signaling by examining the factors directly affected by eROS (Fig. 1). Increasing evidence indicates that signal transduction involves not only the production of eROS but also the regulation of eROS metabolism via various detoxifying enzymes. In addition, various targets of eROS exist extracellularly, where the signal can be indirectly transduced into the cell. The next questions to answer include how the localization and activity of extracellular ROS metabolic enzymes are regulated and how they coordinate with each other to maintain the required ROS level and type. It is also conceivable that ROS generation, turnover, and post-translational modifications of targets may occur within specific compartments. Because such associations outside the cell may not be strong or direct, proximity labeling methods will be useful for revealing the spatial organization of enzyme-target interactions. Given the wide scope of ROS reactions, it would not be possible to ensure target specificity through random diffusion or transport. Understanding the sophisticated spatial control mechanisms for the entire process, from ROS generation to degradation and delivery to the target, represents the next important issue to address.

Figure 1

A diagram showing the multifaceted roles of extracellular reactive oxygen species (eROS).(1) Superoxide (O2•−) produced by RESPIRATORY BURST OXIDASE HOMOLOGs (RBOHs) is converted to hydrogen peroxide (H2O2) by superoxide dismutase ...

Article information

Mol. Cells.Jun 30, 2023; 46(6): 329-336.

Published online 2023-02-17. doi: 10.14348/molcells.2023.2158

Jinsu Lee, Minsoo Han, Yesol Shin, Jung-Min Lee, Geon Heo

¹Research Institute of Basic Sciences, Seoul National University, Seoul 08826, Korea

²School of Biological Sciences, Seoul National University, Seoul 08826, Korea

³Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea

^*Correspondence: yuree.lee@snu.ac.kr

Received October 18, 2022; Accepted December 20, 2022.

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

Articles from Mol. Cells are provided here courtesy of Mol. Cells

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