Redox-dependent control of nuclear transcription in plants

Redox-dependent control of nuclear transcription in plants Abstract Redox-dependent regulatory networks are affected by altered cellular or extracellular levels of reactive oxygen species (ROS). Perturbations of ROS production and scavenging homeostasis have a considerable impact on the nuclear transcriptome. While the regulatory mechanisms by which ROS modulate gene transcription in prokaryotes, lower eukaryotes, and mammalian cells are well established, new insights into the mechanism underlying redox control of gene expression in plants have only recently been known. In this review, we aim to provide an overview of the current knowledge on how ROS and thiol-dependent transcriptional regulatory networks are controlled. We assess the impact of redox perturbations and oxidative stress on transcriptome adjustments using cat2 mutants as a model system and discuss how redox homeostasis can modify the various parts of the transcriptional machinery. Gene expression, glutathione, oxidative stress, plants, reactive oxygen species, redox regulation, transcription factor Introduction The redox state of cells is largely determined by a fine-tuned balance between oxidant production and the antagonistic action of a very proficient, versatile, and flexible antioxidant machinery (Apel and Hirt, 2004; Mittler et al., 2004; Foyer and Noctor, 2009). Reactive oxygen species (ROS) are the most prevalent oxidants and include superoxide oxygen (O2·–), hydrogen peroxide (H2O2), hydroxyl radical (OH·), and singlet oxygen (1O2). These are byproducts of the aerobic metabolism and are produced in different cellular compartments during plant growth and after exposure to stress. Due to their reactivity, ROS can interact with different cell components, such as proteins, nucleic acids, and lipids. To metabolize oxidants, plants have developed ROS-scavenging enzymes the activities of which do or do not rely on reductants, such as catalases (CATs), superoxide dismutases (SODs), ascorbate peroxidases (APXs), glutathione peroxidases (GPXs), and peroxiredoxins (PRXs) (Mittler et al., 2004; Mhamdi et al., 2010a). Among the non-enzymatic antioxidants, the widely distributed hydrophilic redox couples ascorbate/dehydroascorbate (ASC/DHA) and glutathione/glutathione disulfide (GSH/GSSG) are the main redox guardians (Foyer and Noctor, 2011; Noctor et al., 2012). In addition, the plastid-specific tocopherols and carotenoids directly scavenge 1O2 to protect chloroplasts from photo-oxidative events (Fischer et al., 2013). However, under environmental stress conditions, the antioxidant capacity can be overruled by accelerated ROS production or decreased activity of ROS-processing systems that subsequently alter the cell redox homeostasis (referred to as oxidative stress) (Mittler et al., 2004; Mittler, 2017). For instance, under high light, drought, or salinity stress, light absorbed by photosynthetic membranes exceeds the plant’s capacity to assimilate CO2 and overreduces the electron transport chain, causing photoinhibition and increased ROS production in chloroplasts, peroxisomes, and mitochondria (Miller et al., 2010; Dietz, 2015). Upon pathogen infection, plants trigger a rapid and transient production of apoplastic ROS via plasma membrane respiratory burst oxidase homologs (RBOHs) and cell wall peroxidases, termed the ‘oxidative burst’ (Marino et al., 2012). Since their identification as key molecules launching the hypersensitive response and inducing the expression of cellular protectants (Levine et al., 1994), ROS and the associated redox homeostasis are widely accepted to play an important and determining role in triggering appropriate responses to both developmental stimuli and environmental assaults (Schippers et al., 2012; Sewelam et al., 2016; Mittler, 2017, Noctor et al., 2017). Different stresses result in different ROS signatures that might be either sensed directly by redox-sensitive transcription factors (TFs) and receptors or integrated into different signaling pathways to regulate gene expression, translation, and metabolism (Petrov and Van Breusegem, 2012; Foyer and Noctor, 2013; Moore et al., 2016; Willems et al., 2016). Direct effects on proteins targeted by ROS, for example H2O2, imply the modification of the sulfur-containing amino acids, cysteine and methionine. Cysteine residues are first oxidized to sulfenic acid (Cys-SOH). Sulfenic acids, unless they are stabilized into the protein environment, can react rapidly with other protein thiols or with low molecular weight thiols to form intramolecular and intermolecular disulfides. These mechanisms protect the sulfenic acids from overoxidation to sulfinic (SO2H) or sulfonic (SO3H) acid and allow sulfur oxygen signaling (Roos and Messens, 2011; Zagorchev et al., 2013; Waszczak et al., 2015). The oxidized proteins include not only enzymes that directly adjust the cellular metabolism, but also signaling proteins, such as kinases, phosphatases, and TFs, that modulate gene expression (Antelmann and Helmann, 2011; Jacques et al., 2013; Dietz, 2014; Waszczak et al., 2014). Hence, the redox status provides a flexible regulatory system in response to altered conditions. Both thiol proteins and glutathione status act as rheostats in ROS signaling transmission. For example, changes in the glutathione levels induced by increased H2O2 production are required to activate the salicylic acid (SA) signaling pathway (Han et al., 2013). Thioredoxins (TRXs) and glutaredoxins (GRXs) are large thiol oxidoreductase families, comprising mostly a redox center, composed of two essential cysteines that enable them to reduce disulfide bonds in target proteins (Meyer et al., 2012). Changes in the redox state regulated by these reductases can affect protein functions by altering structural properties, enzyme activities, oligomeric states, and interaction partners (Dietz, 2014). This review focuses on the impact of redox and oxidative stress on nuclear gene expression in plants. Increased ROS levels can trigger a broad range of transcriptional changes that initially depend on ROS identity and are regulated ultimately by ROS-responsive elements in the promoters of the responsive genes. First, we present photorespiratory H2O2-modulated transcripts as a case study to discuss the various functional protein categories that are activated by oxidative stress at the transcriptional level. We then discuss known one- and multi-component systems that modulate gene transcription in plants. Although post-transcriptional and epigenetic-related processes, such as chromatin remodeling and small RNAs, are also important regulatory components within the expression of stress-mediated genes, they are not considered here due to space limitation. For a comprehensive overview, we refer the reader to recently published reviews (Shen et al., 2016; Li et al., 2017). ROS-induced transcriptional responses Increased ROS levels are associated with broad transcriptional changes. Over the last decade, microarray and, more recently, RNA-sequencing studies have delivered extensive catalogs of transcriptome-wide changes in transcript abundances during oxidative stress that have facilitated the understanding of the physiological processes involved. To study oxidative stress responses in plants, a range of experimental strategies have been used to enhance cellular oxidant production or to alter redox homeostasis, including (i) direct addition of relatively stable ROS or ROS-generating reagents such as H2O2, methyl viologen (MV), ozone (O3), rotenone, and microbial elicitors (such as flagellin 22); (ii) manipulation of growth conditions, such as high light, CO2 concentration, and stress application as salinity and drought; and (iii) genetic backgrounds affected in ROS metabolism. Arabidopsis thaliana mutants, such as the singlet oxygen-producing fluorescent mutant (flu) and the H2O2-accumulating catalase 2 (cat2), as well as the glutathione synthesis mutants cadmium hypersensitive 2 (cad2) and phytoalexin-deficient mutant 2 (pad2) were useful tools to understand oxidative signaling and to address specific questions related to oxidative stress metabolism and its interaction with other pathways. (Gadjev et al., 2006; Vaahtera et al., 2014; Willems et al., 2016). Transcriptional footprints: indicators of ROS specificity Due to the complex ROS production schemes during environmental stress, different transcriptional responses can be detected. Three main features determine the outcomes of ROS-derived signals: ROS identity, ROS subcellular origin, and exposure time. Each type of ROS has unique chemical properties and, therefore, targets a specific set of signaling routes (Møller et al., 2007; Bindoli and Rigobello, 2013). Whereas OH· reacts rapidly with all types of cellular components, O2·– reacts primarily with the [2Fe–2S]+ protein cluster and 1O2 particularly with conjugated double bonds, as found in polyunsaturated fatty acids (Møller et al., 2007; Sies, 2017). Due to its relative stability and ability to diffuse through membranes, facilitated by aquaporins (Bienert et al., 2007), H2O2 is often considered as a predominant ROS signaling molecule (Levine et al., 1994; Noctor et al., 2002; Petrov and Van Breusegem, 2012). The specificity of ROS-driven transcriptional changes was addressed by several meta-analyses of microarray-based expression data. Marker transcripts that are specifically regulated by H2O2, O2·– and 1O2 as well as a set of general oxidative stress response marker genes, were identified by comparing nine ROS-related microarray experiments (Gadjev et al., 2006). Comparison of O2·– and H2O2-responsive transcripts revealed a considerable overlap which might be explained by the spontaneous or enzymatic dismutation of O2·– to H2O2, while 1O2-responsive transcripts share less overlap with H2O2 and O2·– (Suzuki et al., 2011). Thus, the transcripts solely regulated by either 1O2, O2·–, or H2O2 clearly indicate the existence of distinct signaling pathways for each type of ROS. Despite this, there are no stand-alone units and there is certainly crosstalk between the regulation of the different transcriptional units (Laloi et al., 2007; Willems et al., 2016). In plant cells, a plethora of ROS sources are highly entangled within distinct subcellular compartments that also produce different ROS types (Fig. 1). The apoplastic O2·– is mainly produced by RBOHs and cell wall peroxidases. In chloroplasts, 1O2, O2·–, and H2O2 are produced during photosynthesis, whereas photorespiratory H2O2 is the dominant ROS in the peroxisomes. In mitochondria, O2·– formation is provoked by the overreduction of the respiratory electron transport chain during oxidative phosphorylation and is further dismutated to H2O2 by the mitochondrial SOD. Antioxidants and related enzymes determine the extent of ROS accumulation at different sites and strongly impact the ROS-driven changes in gene expression (Mhamdi et al., 2010b). The ASC–GSH pathway is particularly crucial in this context, as GSH and ASC are used by ROS-processing systems (Fig. 1), and are also able to interact directly with ROS (Foyer and Noctor, 2011; Mittler, 2017). Although each organelle could in theory locally manage its own ROS homeostasis, ROS and related signaling intermediates are certainly also involved in interorganellar communication (Shapiguzov et al., 2012; Mignolet-Spruyt et al., 2016; Noctor and Foyer, 2016). The different oxidative and reductive organellar signals could be first integrated in the cytosol or directly transferred to the nucleus (Fig. 1). Using genetic and transcriptomic approaches, cytosolic enzymes, such as glutathione reductase 1 and APX1, have been demonstrated to be involved particularly in the modulation of the oxidative stress responses (Mhamdi et al., 2010b; Vanderauwera et al., 2011). Furthermore, the dynamic structure of organelles with extensions, such as stromules (chloroplasts), peroxules ( peroxisomes), and matrixules ( mitochondria), allows them to associate physically with the nuclear envelope and directly impinge on the redox state in the nucleus (Noctor and Foyer, 2016). Stromules are formed during innate immunity responses, but can be easily triggered by exogenous application of H2O2, and they facilitated the transfer of plastid proteins and H2O2 into the nucleus (Caplan et al., 2015). A direct transfer of H2O2 from the chloroplast to the nucleus has recently been reported to enable photosynthetic control of gene expression (Exposito-Rodriguez et al., 2017). Fig. 1. View largeDownload slide Overview of ROS and redox signals generated at different subcellular locations and their possible interaction with the nucleus. Signals are integrated into the cytosol and/or transferred to the nucleus. H2O2 can directly be transported from the nucleus to the chloroplasts during the response to high light. APX, ascorbate peroxidase; AQP, aquaporin; ASC, ascorbate; DH, dehydrogenase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; FTR, ferredoxin thioredoxin reductase; GO, glycolate oxidase; GPX, glutathione peroxidase; GR, glutathione reductase; GRX, glutaredoxin; GST, glutathione S-transferase; MDHA, monodehydroascorbate; NTR, NADPH thioredoxin reductase; PETC, photosynthetic electron transfer chain; PRX, peroxiredoxin; RBOH, respiratory burst oxidase homolog; RETC, respiratory electron transport chain; TRXox, oxidized thioredoxin; TRXred, reduced thioredoxin. Fig. 1. View largeDownload slide Overview of ROS and redox signals generated at different subcellular locations and their possible interaction with the nucleus. Signals are integrated into the cytosol and/or transferred to the nucleus. H2O2 can directly be transported from the nucleus to the chloroplasts during the response to high light. APX, ascorbate peroxidase; AQP, aquaporin; ASC, ascorbate; DH, dehydrogenase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; FTR, ferredoxin thioredoxin reductase; GO, glycolate oxidase; GPX, glutathione peroxidase; GR, glutathione reductase; GRX, glutaredoxin; GST, glutathione S-transferase; MDHA, monodehydroascorbate; NTR, NADPH thioredoxin reductase; PETC, photosynthetic electron transfer chain; PRX, peroxiredoxin; RBOH, respiratory burst oxidase homolog; RETC, respiratory electron transport chain; TRXox, oxidized thioredoxin; TRXred, reduced thioredoxin. ROS accumulation during stress can trigger specific changes in the transcriptome in a time-dependent manner. Due to the interaction between different types and pools of ROS, a ROS signal generated by a given stress and at a given time might spread or migrate from the site of origin at later time points to trigger a new homeostatic state (Vaahtera et al., 2014). A recent meta-analysis of transcriptome data revealed that the timing of the oxidative stress treatment was a determining factor in shaping different transcriptome footprints. At later time points, a primary specific stress can converge to more general changes in gene expression (Willems et al., 2016). The complexity of ROS signaling is further illustrated by the interactions between ROS and other signaling pathways, such as SA, jasmonic acid, auxin, ethylene, abscisic acid (ABA), and calcium (Ca2+) signaling (Noctor et al., 2015; Xia et al., 2015). These pathways act together with redox-modulated signaling pathways to process and transmit environmental inputs to produce appropriate responses (Foyer and Noctor, 2009; Noctor et al., 2017). Oxidative stress-responsive cis-regulatory elements (CREs) Control of gene expression depends mainly on the activity of TFs that interact with CREs within the gene promoters. Therefore, CREs can be considered as hardwired molecular switches within a dynamic network that controls gene expression. Various methods allow the identification of CREs, including deletion-based functional analysis, comparative genomics, analysis of co-expressed genes, and ChIP sequencing studies. In mammalian cells, the antioxidant-responsive element (ARE) (TGA[C/T]NNGC) is bound by the NF-E2-related nuclear factors NRF1 and NRF2 that govern the induction of antioxidant defense genes and genes metabolizing xenobiotics, such as UDP-glycosyltransferases (UGTs), multidrug resistance-associated proteins, and glutathione transferases (GSTs), in response to pro-oxidant exposure (Shen and Kong, 2009). However, although the ARE signature is only sporadically reported in plant promoters, AREs are present in the promoters of three maize (Zea mays) CAT genes (Scandalios, 2005) and two wheat (Triticum sp.) GPX genes (Zhai et al., 2013). The identification of CREs specific for different types of ROS addresses the specificity of ROS signaling. In the promoter regions of three antioxidant genes in rice (Oryza sativa), a 28-bp motif designated COORDINATE REGULATORY ELEMENT (CORE) (AANAATNNNTANATAAAANTTTTATNTA) can be activated by the superoxide-inducing MV, but not by H2O2 (Tsukamoto et al., 2005). In a search for Arabidopsis promoter motifs specific for particular types of ROS, seven 1O2-specific and four O2·–-specific motifs were found to be overrepresented in the promoters of the corresponding responsive genes. However, no specific motifs for H2O2 were enriched (Petrov et al., 2012). In addition, some TF-binding motifs were highly represented in promoters of oxidative stress-responsive genes in Arabidopsis, including the W-box (TTGAC/T), recognized by the tryptophan (W)–arginine (R)–lysine (K)–tyrosine (Y) (WRKY) family and the GCC box, recognized by APETALA2/ethylene response factor (AP2/ERF) (Petrov et al., 2012; Wang et al., 2013). In particular, AtERF6 can bind the GCC box specifically to regulate ROS-responsive genes, for instance plant defensin genes (Wang et al., 2013). Another AP2/ERF TF, REDOX RESPONSIVE TRANSCRIPTION FACTOR1 (RRTF1), binds to GCC-box-like sequences in the promoter of genes involved in stress response and redox regulation, for example the zinc finger protein (ZAT) ZAT10 and RELATED TO APETALA (RAP) RAP2.6 TFs (Matsuo et al., 2015). Recently, the GCC box has been shown to be involved in the repression of cytokinin-associated genes in response to oxidative stress via CYTOKININ RESPONSE FACTOR 6, an AP2/ERF TF in Arabidopsis (Zwack et al., 2016). Furthermore, there is crosstalk between ROS and other phytohormones at the promoter level. In the promoter of some Arabidopsis GST genes, an SA- and auxin-responsive element ACTIVATION SEQUENCE-1 (as-1) like motif (TGACG) was found to be activated by ROS (Garretón et al., 2002). The ABA-responsive element (ACGTGTC) was enriched in promoters of the oxidative stress-induced genes in Arabidopsis, indicating the crosstalk between ROS and ABA (Petrov et al., 2012). The ROS-responsive elements were found to regulate leaf senescence. Seven CREs involved in H2O2-mediated control of gene expression during salt stress and senescence were identified by promoter analysis of co-expressed genes in Arabidopsis (Allu et al., 2014), thus suggesting that ROS function as common signaling molecules in both developmental and salt-induced leaf senescence. The CREs involved in mitochondrial retrograde pathways are well studied in Arabidopsis. The binding sites of WRKY, Related to ABA INSENSITIVE 3/VIVIPAROUS 1-A (RAV1-A), basic leucine zipper (bZIP), and myeloblastosis (MYB) TFs were enriched in promoter regions of stress-responsive mitochondrial genes (Van Aken et al., 2009). Later, it was demonstrated that WRKY40 and WRKY63 directly bind to the W-box in promoters of three mitochondrial stress-responsive genes, including ALTERNATIVE OXIDASE 1a (AOX1a) (Van Aken et al., 2013). Furthermore, WRKY TFs play a coordinating role at the interface of both mitochondrial and chloroplast signaling pathways (Van Aken and Whelan, 2012). Besides the known motifs described above, a mitochondrial dysfunction motif (MDM) (CTTGNNNNNCA[AC]G) was identified in a set of genes that coherently respond to perturbed mitochondrial functions (De Clercq et al., 2013). MDM is also sufficient to respond to increased H2O2 levels and is bound by several NAM/ATAF/CUC (NAC) TFs (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078). ANAC017 was also identified as a direct positive regulator of AOX1a in a forward genetic screen, and is necessary for the H2O2-responsive regulation of >85% of the H2O2-responsive genes (Ng et al., 2013). Together with NAC053, ERF6, WRKY6, and NAC032, NAC013 forms an intricate core oxidative stress regulatory network in Arabidopsis (Vermeirssen et al., 2014). ROS-responsive transcripts In plants, the seminal report on an albeit partial genome-wide expression analysis was generated from Arabidopsis cell suspensions harvested 1.5 h and 3 h after treatment with 20 mM H2O2. Using cDNA microarray, 113 and 62 transcripts were induced and repressed, respectively (Desikan et al., 2001). In recent years, using oligonucleotide-based Affymetrix microarrays and RNA-sequencing technologies, transcriptome analyses are much more sensitive and comprehensive and adjustments in plant transcriptomes in response to oxidative stress conditions have been thoroughly documented. Increased ROS levels clearly cause significant changes on plant transcriptomes (Laloi et al., 2007; Short et al., 2012; Queval et al., 2012; Vaahtera et al., 2014; Willems et al., 2016). Peroxisomal photorespiratory H2O2 production was estimated to account for ~70% of the total H2O2 formed at any given irradiance (Noctor et al., 2002). Photorespiratory H2O2 is metabolized firstly by CATs that act as peroxisomal redox guardians (Mhamdi et al., 2012). Loss of CAT activity is associated with increased availability of H2O2 when plants are growing under photorespiration-permissive conditions (Fig. 2A). Therefore, to examine the consequences of an increase in endogenous H2O2, cat2 mutants are a suitable non-invasive in planta system in which perturbation of H2O2 homeostasis is conditional, sustainable over time, and physiologically relevant. Transcriptome analysis of CAT-deficient Arabidopsis and tobacco (Nicotiana tabacum) defined the impact of H2O2 metabolism and photorespiration on gene expression (Vandenabeele et al., 2003, 2004; Vanderauwera et al., 2005). The changes in transcriptome depend on the day length, with the cell death phenotype of cat2 observed only under long-day conditions and associated with induction of defense responses (Queval et al., 2007; Chaouch et al., 2010, 2012). Furthermore, as mentioned above, the cat2 system also allows investigation of the functions of other genes in defining the transcriptome shapes (Mhamdi et al., 2010b; Vanderauwera et al. 2011; Waszczak et al., 2016; Rahantaniaina et al., 2017). Fig. 2. View largeDownload slide Example of oxidative stress-induced transcripts after a 3-h exposure to photorespiratory stress. (A) Elevated H2O2 level in the cat2 mutant under photorespiratory-promoting conditions. (B) Highly induced genes (57) with low (0.1<RPKM<2) to high expression levels (RPKM >100). (C) Emerging genes (128) from absent or very low (RPKM <0.1) to medium expression levels (2<RPKM<100). RPKM, reads per kilobase per million. Fig. 2. View largeDownload slide Example of oxidative stress-induced transcripts after a 3-h exposure to photorespiratory stress. (A) Elevated H2O2 level in the cat2 mutant under photorespiratory-promoting conditions. (B) Highly induced genes (57) with low (0.1<RPKM<2) to high expression levels (RPKM >100). (C) Emerging genes (128) from absent or very low (RPKM <0.1) to medium expression levels (2<RPKM<100). RPKM, reads per kilobase per million. As an illustrative case study of transcriptomic changes induced by increasing intracellular H2O2 levels, we discuss a recently published RNA-sequencing experiment (Kerchev et al., 2016) (Fig. 2). A 3-h high-light exposure under ambient air conditions of cat2 mutants, initially grown at high CO2 concentrations (to block photorespiration), induced and repressed 3571 and 2555 transcripts, respectively ([log2fold change] >1, false discovery rate <0.01). When focusing on transcripts that are barely detectable [0<RPKM (reads per kilobase per million mapped reads) <2] before the increase of H2O2 levels, 57 transcripts are considered to be strongly induced (RPKMs >100) and 128 transcripts moderately induced (2<RPKMs<100; Fig. 2B, C) (the complete list of transcripts is presented in Supplementary Table S1 at JXB online). These transcripts encode proteins of diverse functional categories, including TFs, protein kinases, heat shock proteins (HSPs), GSTs, UGTs, and cytochrome P450 monooxygenases (CYPs). Within the set of 20 TFs, different families are recognized, including WRKY, AP2/ERF, MYB, NAC, heat shock factor (HSF), and ZAT. These stress-related TFs are also up-regulated in a wide range of oxidative stress conditions (Desikan et al., 2001; Vandenabeele et al., 2004; Gadjev et al., 2006; Scarpeci et al., 2008; Balazadeh et al., 2012; Queval et al., 2012). H2O2 treatment in Arabidopsis triggered enhanced expression of several WRKYs (Chen et al., 2010) that control the ROS-dependent responses such as senescence and defense gene expression (Besseau et al., 2012; Guo et al., 2017). The plant-specific AP2/ERF family includes dehydration-responsive element-binding proteins (DREBs), which activate the expression of dehydration- or heat shock-inducible genes (Agarwal et al., 2017). Overexpressors of DREB2C display induced APX gene transcription and confer oxidative stress tolerance to plants (Hwang et al., 2012). RRTF1 induces ROS accumulation in response to stress and its expression is regulated by different WRKYs (Matsuo et al., 2015). In addition, Arabidopsis ZAT12 is responsive to a wide range of stresses, including light, low temperature, wounding and osmotic and oxidative stress, and regulates the expression of oxidative and light stress-responsive genes (e.g. APX1, ZAT7, and WRKY25) (Davletova et al., 2005). The NAC TFs not only steer defense reactions, but also participate in the regulation of ROS metabolism. The drought-responsive NAC WITH TRANSMEMBRANE MOTIF 1-LIKE 4 promotes ROS production during leaf senescence by regulating the RBOH transcript levels, through direct binding to the promoters of the RBOH genes (Lee et al., 2012). In contrast, the H2O2-inducible NAC TF, JUNGBRUNNEN1, negatively regulates leaf senescence by promoting the expression of several HSPs and GSTs (Wu et al., 2012). In a similar context, overexpression of other plant NAC members, such as Arabidopsis NAC013 and rice NAC3, led to tolerance to oxidative stress (De Clercq et al., 2013; Fang et al., 2015). Besides transcriptional regulation, NAC TFs are also regulated at the post-translational level by palmitoylation and phosphorylation (Zhu et al., 2016; Duan et al., 2017). Within the transcripts induced by photorespiratory H2O2, there are 12 protein kinases. In plants, communication between the intracellular and the extracellular environment as well as activation of downstream pathways are largely controlled by receptor-like kinases (RLKs) and receptor-like proteins (Osakabe et al., 2013). RLKs are transmembrane proteins with the N-terminal extracellular region extending into the apoplast where it perceives stimuli, and the C-terminal kinase domain residing inside the cytoplasm and relaying signals into the intracellular environment. The induction of RLKs has been reported in many transcriptome studies (Wrzaczek et al., 2010; Blomster et al., 2011; Kimura et al., 2017), suggesting their importance in facilitating ROS perception and signaling. Among the kinases, oxidative signal inducible kinase 1 (OXI1) is a central protein in ROS sensing that targets mitogen-activated protein kinases (MAPKs) MPK3 and MPK6 to activate defense mechanisms in response to stress, including metal-induced oxidative stress (Smeets et al., 2013). Both gene expression and activity of OXI1 are strongly induced by H2O2 (Rentel et al., 2004). At least 12 small HSPs are strongly up-regulated by photorespiratory H2O2 in this analysis. HSPs are ubiquitous proteins found in plant and mammalian cells, and induced by a wide variety of stresses, including heat, cold, and biotic and abiotic stress (Jacob et al., 2017). Under non-stress conditions, HSPs are key components responsible for protein folding, assembly, translocation, and degradation; under stress conditions, they function in protein stabilization and assist protein refolding (Park and Seo, 2015). The protective function of small HSPs in stress responses is quite conserved among different plant species. Overexpression of three tea (Camellia sinensis) small HSP genes (CsHSP17.7, CsHSP18.1, and CsHSP21.8) confers tolerance to heat and cold stress (Wang et al., 2017). At the mechanistic level, the function of small HSPs is illustrated by AtHSP21, which is required for chloroplast development under heat stress by maintaining plastid-encoded RNA polymerase function (Zhong et al., 2013). The most strongly up-regulated transcripts in cat2 mutants typically include GSTs, UGTs, and CYPs (Queval et al., 2012; Noctor et al., 2015). GSTs are peroxidases and conjugases that use glutathione as substrate and are involved in the metabolism of H2O2 and other peroxides (Dixon and Edwards, 2010). In plants, UGTs are involved in the biosynthesis of plant natural products, such as flavonoids, phenylpropanoids, terpenoids, and steroids, and in the regulation of plant hormones (Bowles et al., 2006). UGTs have been demonstrated to regulate plant growth, abiotic stress and defense responses. Overexpression of AtUGT74E2, encoding an indole-3-butyric acid glycosyltransferase, increased the tolerance to salinity and drought stress in Arabidopsis by regulating auxin homeostasis (Tognetti et al., 2010). Conversely, AtUGT73B2 negatively regulates MV tolerance via glycosylation of flavonoids (Kim et al., 2010). In other detoxification pathways, CYPs are universal enzymes that catalyze the oxidation of various substrates through activation of molecular oxygen. A large group of P450s is responsive to one or several stresses, such as oxidative, osmotic, UV stress, and bacterial and fungal pathogens (Ehlting et al., 2008). In Arabidopsis, the roles of the majority of CYPs remain unknown. In general, genes induced by ROS can be considered to have defense functions, either by orchestrating downstream signaling cascades (e.g. TFs and protein kinases) or by mediating metabolic reactions (e.g. HSPs, UGTs, GSTs, and CYPs). Surprisingly, many members of the core antioxidant system (ROS-processing enzymes) are either not induced or only moderately affected by stress at the transcriptional level (Rossel et al., 2002; Foyer and Noctor, 2009), which might be due to the high expression level even under optimal growth or to tighter control at the post-transcriptional level (Achard et al., 2008; Foyer and Shigeoka, 2011). Hence, it is noteworthy that not only transcription regulation, but also post-transcriptional, translational, and post-translational regulatory mechanisms contribute to the final proteome in response to stress. Redox control of the transcription machinery in oxidative stress One-component systems based on redox-sensitive transcription factors Cysteine residues are sensitive targets of H2O2, as they contain the electron-rich sulfur atom, appearing in a wide range of oxidation states. Various effects can be ascribed to redox changes in cysteine residues, such as conformational changes, subcellular localization, and protein–protein interactions (Antelmann and Helmann, 2011). The simplest redox signaling modules are one-component systems consisting of redox-sensitive TFs. The redox regulation of TFs in plants has been categorized based on the known mechanisms in prokaryotes and non-plant eukaryotes (Dietz, 2014). These mechanisms involve conformational switching, nucleo-cytosolic partitioning, assembly with co-regulators, metal–S cluster regulation, redox control of upstream signaling elements, and proteolysis. An overview of exemplary mechanisms that involve ROS and redox regulation of transcription in plants is presented (Fig. 3) and described in detail below. Fig. 3. View largeDownload slide Redox regulation of TF activity. (A) Redox-regulated conformational switch of NPR1. (B) Four principal redox-sensing mechanisms: (i) conformational change; (ii) association/dissociation with/from a partner; (iii) proteolytic processing; and (iv) DNA binding activity. (C) MAPK pathways in ROS signaling and responses. ROS can activate MPK cascades, thereby activating target genes via phosphorylation or chromatin reprogramming. TR, transcriptional regulator. Fig. 3. View largeDownload slide Redox regulation of TF activity. (A) Redox-regulated conformational switch of NPR1. (B) Four principal redox-sensing mechanisms: (i) conformational change; (ii) association/dissociation with/from a partner; (iii) proteolytic processing; and (iv) DNA binding activity. (C) MAPK pathways in ROS signaling and responses. ROS can activate MPK cascades, thereby activating target genes via phosphorylation or chromatin reprogramming. TR, transcriptional regulator. Redox-dependent changes in the conformational state Many TFs reside in the cytoplasm in an inactive form under non-stress conditions, whereas, upon stress, these are activated and translocated to the nucleus. A well-characterized example of such a regulatory mechanism is the NONEXPRESSOR OF PATHOGENESIS-RELATED GENE 1 (NPR1) that is the master transcriptional co-activator for PATHOGENESIS-RELATED (PR) genes and most other SA-induced genes. Normally, NPR1 is retained in the cytoplasm in an oligomerized oxidized form with intermolecular disulfide bonds involving the residues Cys82 and Cys216 (Mou et al., 2003). In addition, the S-nitrosylation of Cys156 triggers conformational changes of NPR1 assisting disulfide bonds between NPR1 monomers to form inactive oligomers. SA triggers a TRX–H3/H5-dependent reduction of these disulfide bonds, and the monomeric NPR1 migrates to the nucleus (Fig. 3A) (Tada et al., 2008). In the nucleus, monomeric NPR1 interacts with the TGACG sequence-specific binding proteins (TGAs), resulting in the activation of expression of certain genes, particularly the PR genes (Després et al., 2003; Herrera-Vásquez et al., 2015). In addition to redox-sensitive localization dynamics, the activity of NPR1 in the nucleus is tightly regulated by other SA-mediated mechanisms, such as phosphorylation, sumoylation, and proteasome-mediated degradation (Withers and Dong, 2016). Unlike NPR1, HSFs are activated by oxidation rather than reduction [Fig. 3B (i)]. HSFs bind to the conserved heat stress elements (AGAANNTTCT) to activate transcription of HSPs, not only upon heat stress, but also during oxidative stress (Swindell et al., 2007). As shown in Fig. 2, several HSP transcripts are induced by H2O2 in the cat2 background. In plants, several heat stress-induced ROS production sites have been described, mainly including the plasma membrane, apoplast, mitochondria, and chloroplasts (De Pinto et al., 2015). Heat stress-induced H2O2 is required for effective expression of heat shock genes (Volkov et al., 2006). HSFA1A has been shown to be activated via trimerization in response to H2O2in vitro and in vivo (Liu et al., 2013). The redox-dependent translocation from the cytoplasm to the nucleus upon stress has been observed in both HSFA8 and HSFA1D (Jung et al., 2013; Giesguth et al., 2015). The stress-associated protein SAP12 is strongly induced by cold and salinity, and undergoes redox-dependent conformational changes of the quaternary structure (Ströher et al., 2009). Plant-specific DNA-binding WHIRLY1 that can translocate from chloroplasts to the nucleus (Isemer et al., 2012) has been proposed to serve as a redox sensor. Under control conditions, WHIRLY1 forms 24-oligomers that form a bridge between the thylakoid and the nucleoid, whereas upon environmental stimuli, the altered redox state of the photosynthetic apparatus has been proposed to induce a monomerization and translocation of WHIRLY1 into the nucleus (Foyer et al., 2014). Thus, WHIRLY1 might be an ideal candidate for retrograde signaling. Redox control of protein–protein interactions and DNA binding properties The oxidation status of TFs can regulate the association/dissociation of an interacting protein [Fig. 3B (ii)]. Interestingly, the NPR1-interacting TGA TFs that recognize the TGA box are also redox sensitive (Gatz, 2013) and their interaction with NPR1 relies on their redox status. In class I TGAs, an intramolecular disulfide bridge (Cys260–Cys266) precludes interaction with NPR1, and NPR1 can only stimulate DNA binding activity of the reduced form of TGA1 (Després et al., 2003). Class II TGAs, TGA2/6, with only one cysteine residue, interact with GRX480/ROXY19, suggesting that GRX480 control their reduction state (Ndamukong et al., 2007). Redox-mediated modifications can modulate the affinity of TFs towards DNA. The DNA binding activity of RAP2.4A is regulated by dithiol/disulfide transition and subsequent conformational changes. RAP2.4A was identified in a yeast one-hybrid screen for proteins binding to the CRE of the 2-Cys peroxiredoxin A promoter (Shaikhali et al., 2008). The expression of various nuclear-encoded chloroplastic antioxidant enzymes was found to depend on RAP2.4A (Shaikhali et al., 2008; Rudnik et al., 2017). The homodimeric structure of RAP2.4A stabilized by an intermolecular disulfide bond is the active form necessary for DNA binding. Oxidation of the dimer by H2O2 or reduction by DTT strongly reduces its DNA binding affinity (Shaikhali et al., 2008). The oxidation of cysteine residues in the DNA-binding domain might impair the DNA binding activity [Fig. 3B (iv)]. The plant-specific TEOSINTE BRANCHED 1 CYCLOIDEA PCF1 (TCP) TFs are involved in the regulation of developmental processes and hormone responses (Danisman, 2016; Nicolas and Cubas, 2016). The class I TCPs contain a conserved Cys20 located near the DNA-binding domain that upon oxidation inhibits its DNA binding capacities. As TCP15 acts as a repressor of anthocyanin biosynthesis genes, its oxidation and subsequent release from the promoters allow anthocyanin production during long-term high-light exposure (Viola et al., 2013, 2016). Redox sensitivity of a subset of plant R2R3 MYB TFs depends on the presence of a couple of conserved cysteine residues in the R2-MYB motif (Myrset et al., 1993). Maize ZmP1 is a typical R2R3 MYB-domain TF regulating flavonoid biosynthesis via ZmA1. Under oxidizing conditions, the conserved Cys49 and Cys53 residues form an intramolecular disulfide bond inhibiting the binding of ZmP1 to the ZmA1 promoter (Heine et al., 2004). In contrast, Arabidopsis MYB2, which controls salt- and dehydration-responsive genes, has only one conserved cysteine, making the formation of an intramolecular disulfide bond impossible. However, reduction of Cys53 in MYB2 is required for its binding activity and was inhibited by S-nitrosylation (Serpa et al., 2007). The Arabidopsis bZIP16 binds to the high-light-responsive G-box-containing promoter of LIGHT-HARVESTING CHLOROPHYLL A/B-BINDING PROTEIN 2.4 (LHCB2.4). Also here, a conserved cysteine residue was shown to be necessary for redox regulation and enhancement of DNA binding activity and its close homologs bZIP68 and G-BOX BINDING FACTOR 1 (Shaikhali et al., 2012). In sunflower (Helianthus annuus), both HOMEOBOX PROTEIN-10 (HAHB-10) and HAHB ROOT EXPRESSED PROTEIN1 (HAHR1) contain conserved cysteines in the dimerization domains which are associated with the DNA-binding HD domain (Tron et al., 2002). Under reducing conditions, proteins are detected as monomers and exhibit high DNA binding affinity, while under oxidizing conditions they are detected mainly as dimers, suggesting the formation of intermolecular disulfide bonds (Tron et al., 2002). Conservation of cysteines involved in this redox modulation suggests that other plant HD TFs undergo similar changes, as indeed, this was also observed in the Arabidopsis HB-9 (Comelli and Gonzalez, 2007). Redox-mediated proteolysis The activation of TFs through proteolytic release from membranes is illustrated in Fig. 3B (iii). The membrane-anchored TF ANAC089 binds to the promoter of stromal APX. Under reducing conditions, ANAC089 is released from the membrane and translocated to the nucleus (Klein et al., 2012; Yang et al., 2014). Another membrane-anchored NAC TF, ANAC013, undergoes proteolytic activation in response to ROS and moves to the nucleus, where it induces the expression of genes conferring tolerance to oxidative stress induced by MV and rotenone (De Clercq et al., 2013). However, it is not known if the release from the endoplasmic reticulum is directly redox regulated. Similarly, a chloroplast envelope-bound plant homeodomain (PHD) TF with transmembrane domains is involved in regulating chloroplast to nucleus retrograde signals associated with several stress conditions (Sun et al., 2011). When the transmembrane domains are cleaved, PHD accumulates in the nucleus to activate ABI4 expression by direct binding to its promoter. The plant-specific ERFVII TFs have emerged as important regulators, in particular during low-oxygen stress, and are characterized by a conserved N-terminal motif (MCGGAI[I/L]) that function as homeostatic hypoxia sensors via the N-end rule pathway of targeted proteolysis (Gibbs et al., 2011; Licausi et al., 2011). After the removal of the N-terminal methionine by methionine aminopeptidase, the cysteine is exposed and susceptible to oxidative modifications. In the presence of O2 and nitric oxide (NO), cysteine is oxidized to sulfinic or sulfonic acid, subsequently arginylated and recognized by E3 ligase for degradation (Weits et al., 2014). Under hypoxia, limiting oxygen and NO inhibit the N-terminal cysteine oxidation, thus stabilizing the ERFVII TFs and promoting gene expression. Recently, this mechanism has been shown to function as a general sensor of multiple abiotic stresses (Vicente et al., 2017). Multi-component systems utilizing phosphatases and kinases One of the best studied signaling cascades that can directly modulate stress-related TF activities is the MAPK cascade (Jalmi and Sinha, 2015). The MAPK cascade is a well-known signaling module that is conserved from yeast to higher organisms, and activated by various extracellular stimuli, such as pathogen infection, wounding, osmotic stress, cold, and drought. The cascade consists of a MAPK kinase kinase (MKKK) that phosphorylates and activates a MAPK kinase (MKK) which then activates the MAPK by phosphorylation on threonine and tyrosine residues with a conserved domain located in the activation loop of the kinase. Activated MAPKs regulate downstream target genes in several ways, including phosphorylation and regulation of TFs, co-regulatory proteins, and chromatin proteins (Whitmarsh, 2007). MAPK signaling is subjected to redox control and ROS stimuli, and, reciprocally, MAPK cascades regulate redox and ROS homeostasis. Exogenous application of H2O2 can activate a MKKK, ANP1, which initiates a phosphorylation cascade involving MPK3 and MPK6 (Kovtun et al., 2000). The H2O2-responsive OXI1 kinase is required for the full activation of MPK3 and MPK6 (Rentel et al., 2004). The MEKK1 kinase activity and protein stability are regulated by H2O2 and control the ROS-induced MPK4 activation (Nakagami et al., 2006). However, how ROS trigger the MAPK cascade remains to be demonstrated. In mammalian cells, H2O2 oxidizes TRX that interacts with APOPTOSIS SIGNAL-REGULATING KINASE 1 (ASK1). ASK1 subsequently phosphorylates its substrate p38 MAPK (Jarvis et al., 2012). In addition, a cysteine oxidation event in p38 MAPK has been shown to act as a functional regulatory switch (Templeton et al., 2010). In Arabidopsis, in vivo trapping of sulfenylated proteins identified three MAPKs: MPK2, MPK4, and MPK7 (Waszczak et al., 2014), suggesting direct ROS signal perception by MAPK. In rapeseed (Brassica napus), H2O2 has been reported to trigger protein aggregation of BnMPK4 via cysteine oxidation (Zhang et al., 2015). ROS might also activate MAPK by inactivating the MAPK phosphatase (Liu and He, 2017). Various TFs are phosphorylated by MAPKs in response to ROS. In the absence of stress, MPK4 resides in nuclear complexes with WRKY33. Upon stress, WRKY33 is released from MPK4 and targets the promoter of PHYTOALEXIN DEFICIENT 3 (PAD3), which encodes an enzyme required for the synthesis of the phytoalexin camalexin (Qiu et al., 2008). AtERF6 is also a substrate of MPK3/MPK6, and phosphorylation increases the stability of AtERF6 (Meng et al., 2013) and determines changes in ROS-responsive gene transcription via specific binding to the GCC box (Sewelam et al., 2013; Wang et al., 2013; Vogel et al., 2014). Furthermore, HSFA4A is phosphorylated in vitro by MPK3/MPK6 and triggers the transcriptional activation of HSP17.6A (Pérez-Salamó et al., 2014). AtMYB44 is also phosphorylated by MPK3 and, although there is no evidence that the phosphorylation altered the subcellular localization, dimerization, or DNA binding ability of MYB33, it seems to be necessary for an efficient response to abiotic stress (Persak and Pitzschke, 2013). Phosphorylation of MYB75 by MPK4 increases its stability that is required for anthocyanin accumulation in response to light stress (Li et al., 2016). In rice, the salinity- and H2O2-responsive ERF1 is a target of phosphorylation by MPK5, resulting in enhanced transcriptional activation of its target genes containing a DREB-specific cis-element (Schmidt et al., 2013). Redox regulation of the core transcriptional machinery In addition to the stress-specific TFs, the general TFs might also be subject to redox control. In mammalian cells, a member of the TFIIB-like core transcription factor family, TFIIB-related factor 2 (BRF2) facilitating transcription of RNA polymerase (Pol) III, is able specifically to regulate the Pol III transcriptional outputs. Direct redox-sensing functions of BRF2 couple cellular response to oxidative stress and regulation of transcriptional output, contributing to the ability of cancer cells to evade ROS-induced death (Gouge et al., 2015). In plants, topoisomerase VI, which functions in DNA endoreplication, is a key regulatory factor in the activation of ROS-responsive genes and in the modulation of the intensity of the 1O2-induced cell death response (Šimková et al., 2012). The topoisomerase VI binds to the promoter of 1O2-responsive genes and, hence, can directly regulate their expression. Furthermore, enhanced abiotic stress tolerance was observed by overexpressing rice OsTOP6A or OsTOP6B and tobacco NtTOP2 (Jain et al., 2006; John et al., 2016), indicating that topoisomerases might play a role in the integration of multiple ROS signals released by plants in response to environmental stress. The multiprotein complex Mediator is a highly conserved transcriptional co-activator (Bäckström et al., 2007), making the bridge between specific TFs and the RNA polymerase II machinery and hence it converges different signaling pathways before channeling the transcription instructions to the RNA pol II machinery. Evidence for the involvement of the Mediator complex in redox signaling pathways has begun to emerge (Shaikhali et al., 2015). The cysteine-containing Mediator subunits (MED10a, MED28, and MED32) form various types of covalent oligomers linked by intermolecular disulfide bonds that are reduced in vitro by the TRX and GSH–GRX systems. The changes in the redox state of Mediator affect the DNA binding capacity and its interaction with GLABROUS1 ENHANCER-BINDING PROTEIN-LIKE (Shaikhali et al., 2015). The phenotypes of the med28 mutants are characterized by a reduced root length and accelerated leaf senescence. However, whether these phenotypes are linked to the redox changes remains to be investigated (Shaikhali et al., 2016). Concluding remarks and perspectives Redox regulation is integrated into growth, development, and stress-responsive pathways in plants. Perturbations in both ROS production and processing impact significantly on changes in the transcriptome. Evidence compiled from pharmacological and genetic perturbation experiments strongly support these changes as not being part of a generic stress response, but rather forming tailored responses triggered by the individual and spatially organized ROS. To this end, either ROS themselves or secondary signals need to impinge on various regulatory circuits, finally activating or repressing transcriptional regulators and TFs. At this stage, our knowledge of redox-sensitive or redox-responsive transcriptional regulators is still rather scarce. With the advent and implementation of sensitive chemical and protein-based probes that allow discovery of redox-sensitive amino acids in proteins, hopes are high that also in a plant nuclear context, the impact of redox changes and/or oxidative stress on individual proteins and/or complexes will be charted in the future. Redox-active and redox-sensitive organelles, such as chloroplasts, peroxisomes, and mitochondria, can act as central hubs in sensing, relaying, and producing signals towards the nucleus during various environmental stresses. The known signal portfolio currently entails, among others, tetrapyrroles, carotenoid oxidation products, phosphoadenosines, isoprenoid precursors, carbohydrate metabolites, singlet oxygen, and H2O2. Although for both mitochondrial and chloroplastic retrograde signaling, several downstream TFs, target genes, and promoter elements have been identified, the identity of the upstream regulators that transduce the organellar signals into a transcriptional output remains to be discovered, together with the potential involvement of redox-related mechanisms within the perception and transduction events. Alternative pathways through physical contacts between the organelles and the nucleus are emerging, but certainly need to be further validated and explored. One outstanding question is how redox signals are perceived by the transcription machinery and impact gene expression. A set of redox-sensitive TFs has emerged as integration points, as well as signaling pathways such as MAPK. Intriguingly, some components of the core transcription machinery are indicated to function in redox signaling. Although it remains a long journey towards a fully characterized ROS signaling (perception, transduction, and transcription) map, the future elucidation of ROS signaling pathways will certainly be very useful to open up new avenues for breeding stress-tolerant crops. Supplementary data Supplementary data are available at JXB online. Table S1. Expression profiles and categories of strongly and moderately induced transcripts in response to photorespiratory stress Abbreviations Abbreviations ABA abscisic acid APX ascorbate peroxidase bZIP basic leucine zipper CRE cis-regulatory element CYP cytochrome P450 monooxygenase GPX glutathione peroxidase GSH glutathione GSSG glutathione disulfide GST glutathione S-transferase HSF heat shock factor HSP heat shock protein MAPK mitogen-activated protein kinase MV methyl viologen PRX peroxiredoxin PTM post-translational modification RBOH respiratory burst oxidase homolog RLK receptor-like kinase ROS reactive oxygen species SA salicylic acid TF transcription factor TRX thioredoxin UGT UDP-glycosyltransferase Acknowledgements The authors thank Dr Inge De Clercq and Patrick Willems for useful comments on gene expression data analysis, and Dr Martine De Cock for help editing the manuscript. 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Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Botany Oxford University Press

Redox-dependent control of nuclear transcription in plants

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com
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0022-0957
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1460-2431
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10.1093/jxb/ery130
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Abstract

Abstract Redox-dependent regulatory networks are affected by altered cellular or extracellular levels of reactive oxygen species (ROS). Perturbations of ROS production and scavenging homeostasis have a considerable impact on the nuclear transcriptome. While the regulatory mechanisms by which ROS modulate gene transcription in prokaryotes, lower eukaryotes, and mammalian cells are well established, new insights into the mechanism underlying redox control of gene expression in plants have only recently been known. In this review, we aim to provide an overview of the current knowledge on how ROS and thiol-dependent transcriptional regulatory networks are controlled. We assess the impact of redox perturbations and oxidative stress on transcriptome adjustments using cat2 mutants as a model system and discuss how redox homeostasis can modify the various parts of the transcriptional machinery. Gene expression, glutathione, oxidative stress, plants, reactive oxygen species, redox regulation, transcription factor Introduction The redox state of cells is largely determined by a fine-tuned balance between oxidant production and the antagonistic action of a very proficient, versatile, and flexible antioxidant machinery (Apel and Hirt, 2004; Mittler et al., 2004; Foyer and Noctor, 2009). Reactive oxygen species (ROS) are the most prevalent oxidants and include superoxide oxygen (O2·–), hydrogen peroxide (H2O2), hydroxyl radical (OH·), and singlet oxygen (1O2). These are byproducts of the aerobic metabolism and are produced in different cellular compartments during plant growth and after exposure to stress. Due to their reactivity, ROS can interact with different cell components, such as proteins, nucleic acids, and lipids. To metabolize oxidants, plants have developed ROS-scavenging enzymes the activities of which do or do not rely on reductants, such as catalases (CATs), superoxide dismutases (SODs), ascorbate peroxidases (APXs), glutathione peroxidases (GPXs), and peroxiredoxins (PRXs) (Mittler et al., 2004; Mhamdi et al., 2010a). Among the non-enzymatic antioxidants, the widely distributed hydrophilic redox couples ascorbate/dehydroascorbate (ASC/DHA) and glutathione/glutathione disulfide (GSH/GSSG) are the main redox guardians (Foyer and Noctor, 2011; Noctor et al., 2012). In addition, the plastid-specific tocopherols and carotenoids directly scavenge 1O2 to protect chloroplasts from photo-oxidative events (Fischer et al., 2013). However, under environmental stress conditions, the antioxidant capacity can be overruled by accelerated ROS production or decreased activity of ROS-processing systems that subsequently alter the cell redox homeostasis (referred to as oxidative stress) (Mittler et al., 2004; Mittler, 2017). For instance, under high light, drought, or salinity stress, light absorbed by photosynthetic membranes exceeds the plant’s capacity to assimilate CO2 and overreduces the electron transport chain, causing photoinhibition and increased ROS production in chloroplasts, peroxisomes, and mitochondria (Miller et al., 2010; Dietz, 2015). Upon pathogen infection, plants trigger a rapid and transient production of apoplastic ROS via plasma membrane respiratory burst oxidase homologs (RBOHs) and cell wall peroxidases, termed the ‘oxidative burst’ (Marino et al., 2012). Since their identification as key molecules launching the hypersensitive response and inducing the expression of cellular protectants (Levine et al., 1994), ROS and the associated redox homeostasis are widely accepted to play an important and determining role in triggering appropriate responses to both developmental stimuli and environmental assaults (Schippers et al., 2012; Sewelam et al., 2016; Mittler, 2017, Noctor et al., 2017). Different stresses result in different ROS signatures that might be either sensed directly by redox-sensitive transcription factors (TFs) and receptors or integrated into different signaling pathways to regulate gene expression, translation, and metabolism (Petrov and Van Breusegem, 2012; Foyer and Noctor, 2013; Moore et al., 2016; Willems et al., 2016). Direct effects on proteins targeted by ROS, for example H2O2, imply the modification of the sulfur-containing amino acids, cysteine and methionine. Cysteine residues are first oxidized to sulfenic acid (Cys-SOH). Sulfenic acids, unless they are stabilized into the protein environment, can react rapidly with other protein thiols or with low molecular weight thiols to form intramolecular and intermolecular disulfides. These mechanisms protect the sulfenic acids from overoxidation to sulfinic (SO2H) or sulfonic (SO3H) acid and allow sulfur oxygen signaling (Roos and Messens, 2011; Zagorchev et al., 2013; Waszczak et al., 2015). The oxidized proteins include not only enzymes that directly adjust the cellular metabolism, but also signaling proteins, such as kinases, phosphatases, and TFs, that modulate gene expression (Antelmann and Helmann, 2011; Jacques et al., 2013; Dietz, 2014; Waszczak et al., 2014). Hence, the redox status provides a flexible regulatory system in response to altered conditions. Both thiol proteins and glutathione status act as rheostats in ROS signaling transmission. For example, changes in the glutathione levels induced by increased H2O2 production are required to activate the salicylic acid (SA) signaling pathway (Han et al., 2013). Thioredoxins (TRXs) and glutaredoxins (GRXs) are large thiol oxidoreductase families, comprising mostly a redox center, composed of two essential cysteines that enable them to reduce disulfide bonds in target proteins (Meyer et al., 2012). Changes in the redox state regulated by these reductases can affect protein functions by altering structural properties, enzyme activities, oligomeric states, and interaction partners (Dietz, 2014). This review focuses on the impact of redox and oxidative stress on nuclear gene expression in plants. Increased ROS levels can trigger a broad range of transcriptional changes that initially depend on ROS identity and are regulated ultimately by ROS-responsive elements in the promoters of the responsive genes. First, we present photorespiratory H2O2-modulated transcripts as a case study to discuss the various functional protein categories that are activated by oxidative stress at the transcriptional level. We then discuss known one- and multi-component systems that modulate gene transcription in plants. Although post-transcriptional and epigenetic-related processes, such as chromatin remodeling and small RNAs, are also important regulatory components within the expression of stress-mediated genes, they are not considered here due to space limitation. For a comprehensive overview, we refer the reader to recently published reviews (Shen et al., 2016; Li et al., 2017). ROS-induced transcriptional responses Increased ROS levels are associated with broad transcriptional changes. Over the last decade, microarray and, more recently, RNA-sequencing studies have delivered extensive catalogs of transcriptome-wide changes in transcript abundances during oxidative stress that have facilitated the understanding of the physiological processes involved. To study oxidative stress responses in plants, a range of experimental strategies have been used to enhance cellular oxidant production or to alter redox homeostasis, including (i) direct addition of relatively stable ROS or ROS-generating reagents such as H2O2, methyl viologen (MV), ozone (O3), rotenone, and microbial elicitors (such as flagellin 22); (ii) manipulation of growth conditions, such as high light, CO2 concentration, and stress application as salinity and drought; and (iii) genetic backgrounds affected in ROS metabolism. Arabidopsis thaliana mutants, such as the singlet oxygen-producing fluorescent mutant (flu) and the H2O2-accumulating catalase 2 (cat2), as well as the glutathione synthesis mutants cadmium hypersensitive 2 (cad2) and phytoalexin-deficient mutant 2 (pad2) were useful tools to understand oxidative signaling and to address specific questions related to oxidative stress metabolism and its interaction with other pathways. (Gadjev et al., 2006; Vaahtera et al., 2014; Willems et al., 2016). Transcriptional footprints: indicators of ROS specificity Due to the complex ROS production schemes during environmental stress, different transcriptional responses can be detected. Three main features determine the outcomes of ROS-derived signals: ROS identity, ROS subcellular origin, and exposure time. Each type of ROS has unique chemical properties and, therefore, targets a specific set of signaling routes (Møller et al., 2007; Bindoli and Rigobello, 2013). Whereas OH· reacts rapidly with all types of cellular components, O2·– reacts primarily with the [2Fe–2S]+ protein cluster and 1O2 particularly with conjugated double bonds, as found in polyunsaturated fatty acids (Møller et al., 2007; Sies, 2017). Due to its relative stability and ability to diffuse through membranes, facilitated by aquaporins (Bienert et al., 2007), H2O2 is often considered as a predominant ROS signaling molecule (Levine et al., 1994; Noctor et al., 2002; Petrov and Van Breusegem, 2012). The specificity of ROS-driven transcriptional changes was addressed by several meta-analyses of microarray-based expression data. Marker transcripts that are specifically regulated by H2O2, O2·– and 1O2 as well as a set of general oxidative stress response marker genes, were identified by comparing nine ROS-related microarray experiments (Gadjev et al., 2006). Comparison of O2·– and H2O2-responsive transcripts revealed a considerable overlap which might be explained by the spontaneous or enzymatic dismutation of O2·– to H2O2, while 1O2-responsive transcripts share less overlap with H2O2 and O2·– (Suzuki et al., 2011). Thus, the transcripts solely regulated by either 1O2, O2·–, or H2O2 clearly indicate the existence of distinct signaling pathways for each type of ROS. Despite this, there are no stand-alone units and there is certainly crosstalk between the regulation of the different transcriptional units (Laloi et al., 2007; Willems et al., 2016). In plant cells, a plethora of ROS sources are highly entangled within distinct subcellular compartments that also produce different ROS types (Fig. 1). The apoplastic O2·– is mainly produced by RBOHs and cell wall peroxidases. In chloroplasts, 1O2, O2·–, and H2O2 are produced during photosynthesis, whereas photorespiratory H2O2 is the dominant ROS in the peroxisomes. In mitochondria, O2·– formation is provoked by the overreduction of the respiratory electron transport chain during oxidative phosphorylation and is further dismutated to H2O2 by the mitochondrial SOD. Antioxidants and related enzymes determine the extent of ROS accumulation at different sites and strongly impact the ROS-driven changes in gene expression (Mhamdi et al., 2010b). The ASC–GSH pathway is particularly crucial in this context, as GSH and ASC are used by ROS-processing systems (Fig. 1), and are also able to interact directly with ROS (Foyer and Noctor, 2011; Mittler, 2017). Although each organelle could in theory locally manage its own ROS homeostasis, ROS and related signaling intermediates are certainly also involved in interorganellar communication (Shapiguzov et al., 2012; Mignolet-Spruyt et al., 2016; Noctor and Foyer, 2016). The different oxidative and reductive organellar signals could be first integrated in the cytosol or directly transferred to the nucleus (Fig. 1). Using genetic and transcriptomic approaches, cytosolic enzymes, such as glutathione reductase 1 and APX1, have been demonstrated to be involved particularly in the modulation of the oxidative stress responses (Mhamdi et al., 2010b; Vanderauwera et al., 2011). Furthermore, the dynamic structure of organelles with extensions, such as stromules (chloroplasts), peroxules ( peroxisomes), and matrixules ( mitochondria), allows them to associate physically with the nuclear envelope and directly impinge on the redox state in the nucleus (Noctor and Foyer, 2016). Stromules are formed during innate immunity responses, but can be easily triggered by exogenous application of H2O2, and they facilitated the transfer of plastid proteins and H2O2 into the nucleus (Caplan et al., 2015). A direct transfer of H2O2 from the chloroplast to the nucleus has recently been reported to enable photosynthetic control of gene expression (Exposito-Rodriguez et al., 2017). Fig. 1. View largeDownload slide Overview of ROS and redox signals generated at different subcellular locations and their possible interaction with the nucleus. Signals are integrated into the cytosol and/or transferred to the nucleus. H2O2 can directly be transported from the nucleus to the chloroplasts during the response to high light. APX, ascorbate peroxidase; AQP, aquaporin; ASC, ascorbate; DH, dehydrogenase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; FTR, ferredoxin thioredoxin reductase; GO, glycolate oxidase; GPX, glutathione peroxidase; GR, glutathione reductase; GRX, glutaredoxin; GST, glutathione S-transferase; MDHA, monodehydroascorbate; NTR, NADPH thioredoxin reductase; PETC, photosynthetic electron transfer chain; PRX, peroxiredoxin; RBOH, respiratory burst oxidase homolog; RETC, respiratory electron transport chain; TRXox, oxidized thioredoxin; TRXred, reduced thioredoxin. Fig. 1. View largeDownload slide Overview of ROS and redox signals generated at different subcellular locations and their possible interaction with the nucleus. Signals are integrated into the cytosol and/or transferred to the nucleus. H2O2 can directly be transported from the nucleus to the chloroplasts during the response to high light. APX, ascorbate peroxidase; AQP, aquaporin; ASC, ascorbate; DH, dehydrogenase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; FTR, ferredoxin thioredoxin reductase; GO, glycolate oxidase; GPX, glutathione peroxidase; GR, glutathione reductase; GRX, glutaredoxin; GST, glutathione S-transferase; MDHA, monodehydroascorbate; NTR, NADPH thioredoxin reductase; PETC, photosynthetic electron transfer chain; PRX, peroxiredoxin; RBOH, respiratory burst oxidase homolog; RETC, respiratory electron transport chain; TRXox, oxidized thioredoxin; TRXred, reduced thioredoxin. ROS accumulation during stress can trigger specific changes in the transcriptome in a time-dependent manner. Due to the interaction between different types and pools of ROS, a ROS signal generated by a given stress and at a given time might spread or migrate from the site of origin at later time points to trigger a new homeostatic state (Vaahtera et al., 2014). A recent meta-analysis of transcriptome data revealed that the timing of the oxidative stress treatment was a determining factor in shaping different transcriptome footprints. At later time points, a primary specific stress can converge to more general changes in gene expression (Willems et al., 2016). The complexity of ROS signaling is further illustrated by the interactions between ROS and other signaling pathways, such as SA, jasmonic acid, auxin, ethylene, abscisic acid (ABA), and calcium (Ca2+) signaling (Noctor et al., 2015; Xia et al., 2015). These pathways act together with redox-modulated signaling pathways to process and transmit environmental inputs to produce appropriate responses (Foyer and Noctor, 2009; Noctor et al., 2017). Oxidative stress-responsive cis-regulatory elements (CREs) Control of gene expression depends mainly on the activity of TFs that interact with CREs within the gene promoters. Therefore, CREs can be considered as hardwired molecular switches within a dynamic network that controls gene expression. Various methods allow the identification of CREs, including deletion-based functional analysis, comparative genomics, analysis of co-expressed genes, and ChIP sequencing studies. In mammalian cells, the antioxidant-responsive element (ARE) (TGA[C/T]NNGC) is bound by the NF-E2-related nuclear factors NRF1 and NRF2 that govern the induction of antioxidant defense genes and genes metabolizing xenobiotics, such as UDP-glycosyltransferases (UGTs), multidrug resistance-associated proteins, and glutathione transferases (GSTs), in response to pro-oxidant exposure (Shen and Kong, 2009). However, although the ARE signature is only sporadically reported in plant promoters, AREs are present in the promoters of three maize (Zea mays) CAT genes (Scandalios, 2005) and two wheat (Triticum sp.) GPX genes (Zhai et al., 2013). The identification of CREs specific for different types of ROS addresses the specificity of ROS signaling. In the promoter regions of three antioxidant genes in rice (Oryza sativa), a 28-bp motif designated COORDINATE REGULATORY ELEMENT (CORE) (AANAATNNNTANATAAAANTTTTATNTA) can be activated by the superoxide-inducing MV, but not by H2O2 (Tsukamoto et al., 2005). In a search for Arabidopsis promoter motifs specific for particular types of ROS, seven 1O2-specific and four O2·–-specific motifs were found to be overrepresented in the promoters of the corresponding responsive genes. However, no specific motifs for H2O2 were enriched (Petrov et al., 2012). In addition, some TF-binding motifs were highly represented in promoters of oxidative stress-responsive genes in Arabidopsis, including the W-box (TTGAC/T), recognized by the tryptophan (W)–arginine (R)–lysine (K)–tyrosine (Y) (WRKY) family and the GCC box, recognized by APETALA2/ethylene response factor (AP2/ERF) (Petrov et al., 2012; Wang et al., 2013). In particular, AtERF6 can bind the GCC box specifically to regulate ROS-responsive genes, for instance plant defensin genes (Wang et al., 2013). Another AP2/ERF TF, REDOX RESPONSIVE TRANSCRIPTION FACTOR1 (RRTF1), binds to GCC-box-like sequences in the promoter of genes involved in stress response and redox regulation, for example the zinc finger protein (ZAT) ZAT10 and RELATED TO APETALA (RAP) RAP2.6 TFs (Matsuo et al., 2015). Recently, the GCC box has been shown to be involved in the repression of cytokinin-associated genes in response to oxidative stress via CYTOKININ RESPONSE FACTOR 6, an AP2/ERF TF in Arabidopsis (Zwack et al., 2016). Furthermore, there is crosstalk between ROS and other phytohormones at the promoter level. In the promoter of some Arabidopsis GST genes, an SA- and auxin-responsive element ACTIVATION SEQUENCE-1 (as-1) like motif (TGACG) was found to be activated by ROS (Garretón et al., 2002). The ABA-responsive element (ACGTGTC) was enriched in promoters of the oxidative stress-induced genes in Arabidopsis, indicating the crosstalk between ROS and ABA (Petrov et al., 2012). The ROS-responsive elements were found to regulate leaf senescence. Seven CREs involved in H2O2-mediated control of gene expression during salt stress and senescence were identified by promoter analysis of co-expressed genes in Arabidopsis (Allu et al., 2014), thus suggesting that ROS function as common signaling molecules in both developmental and salt-induced leaf senescence. The CREs involved in mitochondrial retrograde pathways are well studied in Arabidopsis. The binding sites of WRKY, Related to ABA INSENSITIVE 3/VIVIPAROUS 1-A (RAV1-A), basic leucine zipper (bZIP), and myeloblastosis (MYB) TFs were enriched in promoter regions of stress-responsive mitochondrial genes (Van Aken et al., 2009). Later, it was demonstrated that WRKY40 and WRKY63 directly bind to the W-box in promoters of three mitochondrial stress-responsive genes, including ALTERNATIVE OXIDASE 1a (AOX1a) (Van Aken et al., 2013). Furthermore, WRKY TFs play a coordinating role at the interface of both mitochondrial and chloroplast signaling pathways (Van Aken and Whelan, 2012). Besides the known motifs described above, a mitochondrial dysfunction motif (MDM) (CTTGNNNNNCA[AC]G) was identified in a set of genes that coherently respond to perturbed mitochondrial functions (De Clercq et al., 2013). MDM is also sufficient to respond to increased H2O2 levels and is bound by several NAM/ATAF/CUC (NAC) TFs (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078). ANAC017 was also identified as a direct positive regulator of AOX1a in a forward genetic screen, and is necessary for the H2O2-responsive regulation of >85% of the H2O2-responsive genes (Ng et al., 2013). Together with NAC053, ERF6, WRKY6, and NAC032, NAC013 forms an intricate core oxidative stress regulatory network in Arabidopsis (Vermeirssen et al., 2014). ROS-responsive transcripts In plants, the seminal report on an albeit partial genome-wide expression analysis was generated from Arabidopsis cell suspensions harvested 1.5 h and 3 h after treatment with 20 mM H2O2. Using cDNA microarray, 113 and 62 transcripts were induced and repressed, respectively (Desikan et al., 2001). In recent years, using oligonucleotide-based Affymetrix microarrays and RNA-sequencing technologies, transcriptome analyses are much more sensitive and comprehensive and adjustments in plant transcriptomes in response to oxidative stress conditions have been thoroughly documented. Increased ROS levels clearly cause significant changes on plant transcriptomes (Laloi et al., 2007; Short et al., 2012; Queval et al., 2012; Vaahtera et al., 2014; Willems et al., 2016). Peroxisomal photorespiratory H2O2 production was estimated to account for ~70% of the total H2O2 formed at any given irradiance (Noctor et al., 2002). Photorespiratory H2O2 is metabolized firstly by CATs that act as peroxisomal redox guardians (Mhamdi et al., 2012). Loss of CAT activity is associated with increased availability of H2O2 when plants are growing under photorespiration-permissive conditions (Fig. 2A). Therefore, to examine the consequences of an increase in endogenous H2O2, cat2 mutants are a suitable non-invasive in planta system in which perturbation of H2O2 homeostasis is conditional, sustainable over time, and physiologically relevant. Transcriptome analysis of CAT-deficient Arabidopsis and tobacco (Nicotiana tabacum) defined the impact of H2O2 metabolism and photorespiration on gene expression (Vandenabeele et al., 2003, 2004; Vanderauwera et al., 2005). The changes in transcriptome depend on the day length, with the cell death phenotype of cat2 observed only under long-day conditions and associated with induction of defense responses (Queval et al., 2007; Chaouch et al., 2010, 2012). Furthermore, as mentioned above, the cat2 system also allows investigation of the functions of other genes in defining the transcriptome shapes (Mhamdi et al., 2010b; Vanderauwera et al. 2011; Waszczak et al., 2016; Rahantaniaina et al., 2017). Fig. 2. View largeDownload slide Example of oxidative stress-induced transcripts after a 3-h exposure to photorespiratory stress. (A) Elevated H2O2 level in the cat2 mutant under photorespiratory-promoting conditions. (B) Highly induced genes (57) with low (0.1<RPKM<2) to high expression levels (RPKM >100). (C) Emerging genes (128) from absent or very low (RPKM <0.1) to medium expression levels (2<RPKM<100). RPKM, reads per kilobase per million. Fig. 2. View largeDownload slide Example of oxidative stress-induced transcripts after a 3-h exposure to photorespiratory stress. (A) Elevated H2O2 level in the cat2 mutant under photorespiratory-promoting conditions. (B) Highly induced genes (57) with low (0.1<RPKM<2) to high expression levels (RPKM >100). (C) Emerging genes (128) from absent or very low (RPKM <0.1) to medium expression levels (2<RPKM<100). RPKM, reads per kilobase per million. As an illustrative case study of transcriptomic changes induced by increasing intracellular H2O2 levels, we discuss a recently published RNA-sequencing experiment (Kerchev et al., 2016) (Fig. 2). A 3-h high-light exposure under ambient air conditions of cat2 mutants, initially grown at high CO2 concentrations (to block photorespiration), induced and repressed 3571 and 2555 transcripts, respectively ([log2fold change] >1, false discovery rate <0.01). When focusing on transcripts that are barely detectable [0<RPKM (reads per kilobase per million mapped reads) <2] before the increase of H2O2 levels, 57 transcripts are considered to be strongly induced (RPKMs >100) and 128 transcripts moderately induced (2<RPKMs<100; Fig. 2B, C) (the complete list of transcripts is presented in Supplementary Table S1 at JXB online). These transcripts encode proteins of diverse functional categories, including TFs, protein kinases, heat shock proteins (HSPs), GSTs, UGTs, and cytochrome P450 monooxygenases (CYPs). Within the set of 20 TFs, different families are recognized, including WRKY, AP2/ERF, MYB, NAC, heat shock factor (HSF), and ZAT. These stress-related TFs are also up-regulated in a wide range of oxidative stress conditions (Desikan et al., 2001; Vandenabeele et al., 2004; Gadjev et al., 2006; Scarpeci et al., 2008; Balazadeh et al., 2012; Queval et al., 2012). H2O2 treatment in Arabidopsis triggered enhanced expression of several WRKYs (Chen et al., 2010) that control the ROS-dependent responses such as senescence and defense gene expression (Besseau et al., 2012; Guo et al., 2017). The plant-specific AP2/ERF family includes dehydration-responsive element-binding proteins (DREBs), which activate the expression of dehydration- or heat shock-inducible genes (Agarwal et al., 2017). Overexpressors of DREB2C display induced APX gene transcription and confer oxidative stress tolerance to plants (Hwang et al., 2012). RRTF1 induces ROS accumulation in response to stress and its expression is regulated by different WRKYs (Matsuo et al., 2015). In addition, Arabidopsis ZAT12 is responsive to a wide range of stresses, including light, low temperature, wounding and osmotic and oxidative stress, and regulates the expression of oxidative and light stress-responsive genes (e.g. APX1, ZAT7, and WRKY25) (Davletova et al., 2005). The NAC TFs not only steer defense reactions, but also participate in the regulation of ROS metabolism. The drought-responsive NAC WITH TRANSMEMBRANE MOTIF 1-LIKE 4 promotes ROS production during leaf senescence by regulating the RBOH transcript levels, through direct binding to the promoters of the RBOH genes (Lee et al., 2012). In contrast, the H2O2-inducible NAC TF, JUNGBRUNNEN1, negatively regulates leaf senescence by promoting the expression of several HSPs and GSTs (Wu et al., 2012). In a similar context, overexpression of other plant NAC members, such as Arabidopsis NAC013 and rice NAC3, led to tolerance to oxidative stress (De Clercq et al., 2013; Fang et al., 2015). Besides transcriptional regulation, NAC TFs are also regulated at the post-translational level by palmitoylation and phosphorylation (Zhu et al., 2016; Duan et al., 2017). Within the transcripts induced by photorespiratory H2O2, there are 12 protein kinases. In plants, communication between the intracellular and the extracellular environment as well as activation of downstream pathways are largely controlled by receptor-like kinases (RLKs) and receptor-like proteins (Osakabe et al., 2013). RLKs are transmembrane proteins with the N-terminal extracellular region extending into the apoplast where it perceives stimuli, and the C-terminal kinase domain residing inside the cytoplasm and relaying signals into the intracellular environment. The induction of RLKs has been reported in many transcriptome studies (Wrzaczek et al., 2010; Blomster et al., 2011; Kimura et al., 2017), suggesting their importance in facilitating ROS perception and signaling. Among the kinases, oxidative signal inducible kinase 1 (OXI1) is a central protein in ROS sensing that targets mitogen-activated protein kinases (MAPKs) MPK3 and MPK6 to activate defense mechanisms in response to stress, including metal-induced oxidative stress (Smeets et al., 2013). Both gene expression and activity of OXI1 are strongly induced by H2O2 (Rentel et al., 2004). At least 12 small HSPs are strongly up-regulated by photorespiratory H2O2 in this analysis. HSPs are ubiquitous proteins found in plant and mammalian cells, and induced by a wide variety of stresses, including heat, cold, and biotic and abiotic stress (Jacob et al., 2017). Under non-stress conditions, HSPs are key components responsible for protein folding, assembly, translocation, and degradation; under stress conditions, they function in protein stabilization and assist protein refolding (Park and Seo, 2015). The protective function of small HSPs in stress responses is quite conserved among different plant species. Overexpression of three tea (Camellia sinensis) small HSP genes (CsHSP17.7, CsHSP18.1, and CsHSP21.8) confers tolerance to heat and cold stress (Wang et al., 2017). At the mechanistic level, the function of small HSPs is illustrated by AtHSP21, which is required for chloroplast development under heat stress by maintaining plastid-encoded RNA polymerase function (Zhong et al., 2013). The most strongly up-regulated transcripts in cat2 mutants typically include GSTs, UGTs, and CYPs (Queval et al., 2012; Noctor et al., 2015). GSTs are peroxidases and conjugases that use glutathione as substrate and are involved in the metabolism of H2O2 and other peroxides (Dixon and Edwards, 2010). In plants, UGTs are involved in the biosynthesis of plant natural products, such as flavonoids, phenylpropanoids, terpenoids, and steroids, and in the regulation of plant hormones (Bowles et al., 2006). UGTs have been demonstrated to regulate plant growth, abiotic stress and defense responses. Overexpression of AtUGT74E2, encoding an indole-3-butyric acid glycosyltransferase, increased the tolerance to salinity and drought stress in Arabidopsis by regulating auxin homeostasis (Tognetti et al., 2010). Conversely, AtUGT73B2 negatively regulates MV tolerance via glycosylation of flavonoids (Kim et al., 2010). In other detoxification pathways, CYPs are universal enzymes that catalyze the oxidation of various substrates through activation of molecular oxygen. A large group of P450s is responsive to one or several stresses, such as oxidative, osmotic, UV stress, and bacterial and fungal pathogens (Ehlting et al., 2008). In Arabidopsis, the roles of the majority of CYPs remain unknown. In general, genes induced by ROS can be considered to have defense functions, either by orchestrating downstream signaling cascades (e.g. TFs and protein kinases) or by mediating metabolic reactions (e.g. HSPs, UGTs, GSTs, and CYPs). Surprisingly, many members of the core antioxidant system (ROS-processing enzymes) are either not induced or only moderately affected by stress at the transcriptional level (Rossel et al., 2002; Foyer and Noctor, 2009), which might be due to the high expression level even under optimal growth or to tighter control at the post-transcriptional level (Achard et al., 2008; Foyer and Shigeoka, 2011). Hence, it is noteworthy that not only transcription regulation, but also post-transcriptional, translational, and post-translational regulatory mechanisms contribute to the final proteome in response to stress. Redox control of the transcription machinery in oxidative stress One-component systems based on redox-sensitive transcription factors Cysteine residues are sensitive targets of H2O2, as they contain the electron-rich sulfur atom, appearing in a wide range of oxidation states. Various effects can be ascribed to redox changes in cysteine residues, such as conformational changes, subcellular localization, and protein–protein interactions (Antelmann and Helmann, 2011). The simplest redox signaling modules are one-component systems consisting of redox-sensitive TFs. The redox regulation of TFs in plants has been categorized based on the known mechanisms in prokaryotes and non-plant eukaryotes (Dietz, 2014). These mechanisms involve conformational switching, nucleo-cytosolic partitioning, assembly with co-regulators, metal–S cluster regulation, redox control of upstream signaling elements, and proteolysis. An overview of exemplary mechanisms that involve ROS and redox regulation of transcription in plants is presented (Fig. 3) and described in detail below. Fig. 3. View largeDownload slide Redox regulation of TF activity. (A) Redox-regulated conformational switch of NPR1. (B) Four principal redox-sensing mechanisms: (i) conformational change; (ii) association/dissociation with/from a partner; (iii) proteolytic processing; and (iv) DNA binding activity. (C) MAPK pathways in ROS signaling and responses. ROS can activate MPK cascades, thereby activating target genes via phosphorylation or chromatin reprogramming. TR, transcriptional regulator. Fig. 3. View largeDownload slide Redox regulation of TF activity. (A) Redox-regulated conformational switch of NPR1. (B) Four principal redox-sensing mechanisms: (i) conformational change; (ii) association/dissociation with/from a partner; (iii) proteolytic processing; and (iv) DNA binding activity. (C) MAPK pathways in ROS signaling and responses. ROS can activate MPK cascades, thereby activating target genes via phosphorylation or chromatin reprogramming. TR, transcriptional regulator. Redox-dependent changes in the conformational state Many TFs reside in the cytoplasm in an inactive form under non-stress conditions, whereas, upon stress, these are activated and translocated to the nucleus. A well-characterized example of such a regulatory mechanism is the NONEXPRESSOR OF PATHOGENESIS-RELATED GENE 1 (NPR1) that is the master transcriptional co-activator for PATHOGENESIS-RELATED (PR) genes and most other SA-induced genes. Normally, NPR1 is retained in the cytoplasm in an oligomerized oxidized form with intermolecular disulfide bonds involving the residues Cys82 and Cys216 (Mou et al., 2003). In addition, the S-nitrosylation of Cys156 triggers conformational changes of NPR1 assisting disulfide bonds between NPR1 monomers to form inactive oligomers. SA triggers a TRX–H3/H5-dependent reduction of these disulfide bonds, and the monomeric NPR1 migrates to the nucleus (Fig. 3A) (Tada et al., 2008). In the nucleus, monomeric NPR1 interacts with the TGACG sequence-specific binding proteins (TGAs), resulting in the activation of expression of certain genes, particularly the PR genes (Després et al., 2003; Herrera-Vásquez et al., 2015). In addition to redox-sensitive localization dynamics, the activity of NPR1 in the nucleus is tightly regulated by other SA-mediated mechanisms, such as phosphorylation, sumoylation, and proteasome-mediated degradation (Withers and Dong, 2016). Unlike NPR1, HSFs are activated by oxidation rather than reduction [Fig. 3B (i)]. HSFs bind to the conserved heat stress elements (AGAANNTTCT) to activate transcription of HSPs, not only upon heat stress, but also during oxidative stress (Swindell et al., 2007). As shown in Fig. 2, several HSP transcripts are induced by H2O2 in the cat2 background. In plants, several heat stress-induced ROS production sites have been described, mainly including the plasma membrane, apoplast, mitochondria, and chloroplasts (De Pinto et al., 2015). Heat stress-induced H2O2 is required for effective expression of heat shock genes (Volkov et al., 2006). HSFA1A has been shown to be activated via trimerization in response to H2O2in vitro and in vivo (Liu et al., 2013). The redox-dependent translocation from the cytoplasm to the nucleus upon stress has been observed in both HSFA8 and HSFA1D (Jung et al., 2013; Giesguth et al., 2015). The stress-associated protein SAP12 is strongly induced by cold and salinity, and undergoes redox-dependent conformational changes of the quaternary structure (Ströher et al., 2009). Plant-specific DNA-binding WHIRLY1 that can translocate from chloroplasts to the nucleus (Isemer et al., 2012) has been proposed to serve as a redox sensor. Under control conditions, WHIRLY1 forms 24-oligomers that form a bridge between the thylakoid and the nucleoid, whereas upon environmental stimuli, the altered redox state of the photosynthetic apparatus has been proposed to induce a monomerization and translocation of WHIRLY1 into the nucleus (Foyer et al., 2014). Thus, WHIRLY1 might be an ideal candidate for retrograde signaling. Redox control of protein–protein interactions and DNA binding properties The oxidation status of TFs can regulate the association/dissociation of an interacting protein [Fig. 3B (ii)]. Interestingly, the NPR1-interacting TGA TFs that recognize the TGA box are also redox sensitive (Gatz, 2013) and their interaction with NPR1 relies on their redox status. In class I TGAs, an intramolecular disulfide bridge (Cys260–Cys266) precludes interaction with NPR1, and NPR1 can only stimulate DNA binding activity of the reduced form of TGA1 (Després et al., 2003). Class II TGAs, TGA2/6, with only one cysteine residue, interact with GRX480/ROXY19, suggesting that GRX480 control their reduction state (Ndamukong et al., 2007). Redox-mediated modifications can modulate the affinity of TFs towards DNA. The DNA binding activity of RAP2.4A is regulated by dithiol/disulfide transition and subsequent conformational changes. RAP2.4A was identified in a yeast one-hybrid screen for proteins binding to the CRE of the 2-Cys peroxiredoxin A promoter (Shaikhali et al., 2008). The expression of various nuclear-encoded chloroplastic antioxidant enzymes was found to depend on RAP2.4A (Shaikhali et al., 2008; Rudnik et al., 2017). The homodimeric structure of RAP2.4A stabilized by an intermolecular disulfide bond is the active form necessary for DNA binding. Oxidation of the dimer by H2O2 or reduction by DTT strongly reduces its DNA binding affinity (Shaikhali et al., 2008). The oxidation of cysteine residues in the DNA-binding domain might impair the DNA binding activity [Fig. 3B (iv)]. The plant-specific TEOSINTE BRANCHED 1 CYCLOIDEA PCF1 (TCP) TFs are involved in the regulation of developmental processes and hormone responses (Danisman, 2016; Nicolas and Cubas, 2016). The class I TCPs contain a conserved Cys20 located near the DNA-binding domain that upon oxidation inhibits its DNA binding capacities. As TCP15 acts as a repressor of anthocyanin biosynthesis genes, its oxidation and subsequent release from the promoters allow anthocyanin production during long-term high-light exposure (Viola et al., 2013, 2016). Redox sensitivity of a subset of plant R2R3 MYB TFs depends on the presence of a couple of conserved cysteine residues in the R2-MYB motif (Myrset et al., 1993). Maize ZmP1 is a typical R2R3 MYB-domain TF regulating flavonoid biosynthesis via ZmA1. Under oxidizing conditions, the conserved Cys49 and Cys53 residues form an intramolecular disulfide bond inhibiting the binding of ZmP1 to the ZmA1 promoter (Heine et al., 2004). In contrast, Arabidopsis MYB2, which controls salt- and dehydration-responsive genes, has only one conserved cysteine, making the formation of an intramolecular disulfide bond impossible. However, reduction of Cys53 in MYB2 is required for its binding activity and was inhibited by S-nitrosylation (Serpa et al., 2007). The Arabidopsis bZIP16 binds to the high-light-responsive G-box-containing promoter of LIGHT-HARVESTING CHLOROPHYLL A/B-BINDING PROTEIN 2.4 (LHCB2.4). Also here, a conserved cysteine residue was shown to be necessary for redox regulation and enhancement of DNA binding activity and its close homologs bZIP68 and G-BOX BINDING FACTOR 1 (Shaikhali et al., 2012). In sunflower (Helianthus annuus), both HOMEOBOX PROTEIN-10 (HAHB-10) and HAHB ROOT EXPRESSED PROTEIN1 (HAHR1) contain conserved cysteines in the dimerization domains which are associated with the DNA-binding HD domain (Tron et al., 2002). Under reducing conditions, proteins are detected as monomers and exhibit high DNA binding affinity, while under oxidizing conditions they are detected mainly as dimers, suggesting the formation of intermolecular disulfide bonds (Tron et al., 2002). Conservation of cysteines involved in this redox modulation suggests that other plant HD TFs undergo similar changes, as indeed, this was also observed in the Arabidopsis HB-9 (Comelli and Gonzalez, 2007). Redox-mediated proteolysis The activation of TFs through proteolytic release from membranes is illustrated in Fig. 3B (iii). The membrane-anchored TF ANAC089 binds to the promoter of stromal APX. Under reducing conditions, ANAC089 is released from the membrane and translocated to the nucleus (Klein et al., 2012; Yang et al., 2014). Another membrane-anchored NAC TF, ANAC013, undergoes proteolytic activation in response to ROS and moves to the nucleus, where it induces the expression of genes conferring tolerance to oxidative stress induced by MV and rotenone (De Clercq et al., 2013). However, it is not known if the release from the endoplasmic reticulum is directly redox regulated. Similarly, a chloroplast envelope-bound plant homeodomain (PHD) TF with transmembrane domains is involved in regulating chloroplast to nucleus retrograde signals associated with several stress conditions (Sun et al., 2011). When the transmembrane domains are cleaved, PHD accumulates in the nucleus to activate ABI4 expression by direct binding to its promoter. The plant-specific ERFVII TFs have emerged as important regulators, in particular during low-oxygen stress, and are characterized by a conserved N-terminal motif (MCGGAI[I/L]) that function as homeostatic hypoxia sensors via the N-end rule pathway of targeted proteolysis (Gibbs et al., 2011; Licausi et al., 2011). After the removal of the N-terminal methionine by methionine aminopeptidase, the cysteine is exposed and susceptible to oxidative modifications. In the presence of O2 and nitric oxide (NO), cysteine is oxidized to sulfinic or sulfonic acid, subsequently arginylated and recognized by E3 ligase for degradation (Weits et al., 2014). Under hypoxia, limiting oxygen and NO inhibit the N-terminal cysteine oxidation, thus stabilizing the ERFVII TFs and promoting gene expression. Recently, this mechanism has been shown to function as a general sensor of multiple abiotic stresses (Vicente et al., 2017). Multi-component systems utilizing phosphatases and kinases One of the best studied signaling cascades that can directly modulate stress-related TF activities is the MAPK cascade (Jalmi and Sinha, 2015). The MAPK cascade is a well-known signaling module that is conserved from yeast to higher organisms, and activated by various extracellular stimuli, such as pathogen infection, wounding, osmotic stress, cold, and drought. The cascade consists of a MAPK kinase kinase (MKKK) that phosphorylates and activates a MAPK kinase (MKK) which then activates the MAPK by phosphorylation on threonine and tyrosine residues with a conserved domain located in the activation loop of the kinase. Activated MAPKs regulate downstream target genes in several ways, including phosphorylation and regulation of TFs, co-regulatory proteins, and chromatin proteins (Whitmarsh, 2007). MAPK signaling is subjected to redox control and ROS stimuli, and, reciprocally, MAPK cascades regulate redox and ROS homeostasis. Exogenous application of H2O2 can activate a MKKK, ANP1, which initiates a phosphorylation cascade involving MPK3 and MPK6 (Kovtun et al., 2000). The H2O2-responsive OXI1 kinase is required for the full activation of MPK3 and MPK6 (Rentel et al., 2004). The MEKK1 kinase activity and protein stability are regulated by H2O2 and control the ROS-induced MPK4 activation (Nakagami et al., 2006). However, how ROS trigger the MAPK cascade remains to be demonstrated. In mammalian cells, H2O2 oxidizes TRX that interacts with APOPTOSIS SIGNAL-REGULATING KINASE 1 (ASK1). ASK1 subsequently phosphorylates its substrate p38 MAPK (Jarvis et al., 2012). In addition, a cysteine oxidation event in p38 MAPK has been shown to act as a functional regulatory switch (Templeton et al., 2010). In Arabidopsis, in vivo trapping of sulfenylated proteins identified three MAPKs: MPK2, MPK4, and MPK7 (Waszczak et al., 2014), suggesting direct ROS signal perception by MAPK. In rapeseed (Brassica napus), H2O2 has been reported to trigger protein aggregation of BnMPK4 via cysteine oxidation (Zhang et al., 2015). ROS might also activate MAPK by inactivating the MAPK phosphatase (Liu and He, 2017). Various TFs are phosphorylated by MAPKs in response to ROS. In the absence of stress, MPK4 resides in nuclear complexes with WRKY33. Upon stress, WRKY33 is released from MPK4 and targets the promoter of PHYTOALEXIN DEFICIENT 3 (PAD3), which encodes an enzyme required for the synthesis of the phytoalexin camalexin (Qiu et al., 2008). AtERF6 is also a substrate of MPK3/MPK6, and phosphorylation increases the stability of AtERF6 (Meng et al., 2013) and determines changes in ROS-responsive gene transcription via specific binding to the GCC box (Sewelam et al., 2013; Wang et al., 2013; Vogel et al., 2014). Furthermore, HSFA4A is phosphorylated in vitro by MPK3/MPK6 and triggers the transcriptional activation of HSP17.6A (Pérez-Salamó et al., 2014). AtMYB44 is also phosphorylated by MPK3 and, although there is no evidence that the phosphorylation altered the subcellular localization, dimerization, or DNA binding ability of MYB33, it seems to be necessary for an efficient response to abiotic stress (Persak and Pitzschke, 2013). Phosphorylation of MYB75 by MPK4 increases its stability that is required for anthocyanin accumulation in response to light stress (Li et al., 2016). In rice, the salinity- and H2O2-responsive ERF1 is a target of phosphorylation by MPK5, resulting in enhanced transcriptional activation of its target genes containing a DREB-specific cis-element (Schmidt et al., 2013). Redox regulation of the core transcriptional machinery In addition to the stress-specific TFs, the general TFs might also be subject to redox control. In mammalian cells, a member of the TFIIB-like core transcription factor family, TFIIB-related factor 2 (BRF2) facilitating transcription of RNA polymerase (Pol) III, is able specifically to regulate the Pol III transcriptional outputs. Direct redox-sensing functions of BRF2 couple cellular response to oxidative stress and regulation of transcriptional output, contributing to the ability of cancer cells to evade ROS-induced death (Gouge et al., 2015). In plants, topoisomerase VI, which functions in DNA endoreplication, is a key regulatory factor in the activation of ROS-responsive genes and in the modulation of the intensity of the 1O2-induced cell death response (Šimková et al., 2012). The topoisomerase VI binds to the promoter of 1O2-responsive genes and, hence, can directly regulate their expression. Furthermore, enhanced abiotic stress tolerance was observed by overexpressing rice OsTOP6A or OsTOP6B and tobacco NtTOP2 (Jain et al., 2006; John et al., 2016), indicating that topoisomerases might play a role in the integration of multiple ROS signals released by plants in response to environmental stress. The multiprotein complex Mediator is a highly conserved transcriptional co-activator (Bäckström et al., 2007), making the bridge between specific TFs and the RNA polymerase II machinery and hence it converges different signaling pathways before channeling the transcription instructions to the RNA pol II machinery. Evidence for the involvement of the Mediator complex in redox signaling pathways has begun to emerge (Shaikhali et al., 2015). The cysteine-containing Mediator subunits (MED10a, MED28, and MED32) form various types of covalent oligomers linked by intermolecular disulfide bonds that are reduced in vitro by the TRX and GSH–GRX systems. The changes in the redox state of Mediator affect the DNA binding capacity and its interaction with GLABROUS1 ENHANCER-BINDING PROTEIN-LIKE (Shaikhali et al., 2015). The phenotypes of the med28 mutants are characterized by a reduced root length and accelerated leaf senescence. However, whether these phenotypes are linked to the redox changes remains to be investigated (Shaikhali et al., 2016). Concluding remarks and perspectives Redox regulation is integrated into growth, development, and stress-responsive pathways in plants. Perturbations in both ROS production and processing impact significantly on changes in the transcriptome. Evidence compiled from pharmacological and genetic perturbation experiments strongly support these changes as not being part of a generic stress response, but rather forming tailored responses triggered by the individual and spatially organized ROS. To this end, either ROS themselves or secondary signals need to impinge on various regulatory circuits, finally activating or repressing transcriptional regulators and TFs. At this stage, our knowledge of redox-sensitive or redox-responsive transcriptional regulators is still rather scarce. With the advent and implementation of sensitive chemical and protein-based probes that allow discovery of redox-sensitive amino acids in proteins, hopes are high that also in a plant nuclear context, the impact of redox changes and/or oxidative stress on individual proteins and/or complexes will be charted in the future. Redox-active and redox-sensitive organelles, such as chloroplasts, peroxisomes, and mitochondria, can act as central hubs in sensing, relaying, and producing signals towards the nucleus during various environmental stresses. The known signal portfolio currently entails, among others, tetrapyrroles, carotenoid oxidation products, phosphoadenosines, isoprenoid precursors, carbohydrate metabolites, singlet oxygen, and H2O2. Although for both mitochondrial and chloroplastic retrograde signaling, several downstream TFs, target genes, and promoter elements have been identified, the identity of the upstream regulators that transduce the organellar signals into a transcriptional output remains to be discovered, together with the potential involvement of redox-related mechanisms within the perception and transduction events. Alternative pathways through physical contacts between the organelles and the nucleus are emerging, but certainly need to be further validated and explored. One outstanding question is how redox signals are perceived by the transcription machinery and impact gene expression. A set of redox-sensitive TFs has emerged as integration points, as well as signaling pathways such as MAPK. Intriguingly, some components of the core transcription machinery are indicated to function in redox signaling. Although it remains a long journey towards a fully characterized ROS signaling (perception, transduction, and transcription) map, the future elucidation of ROS signaling pathways will certainly be very useful to open up new avenues for breeding stress-tolerant crops. Supplementary data Supplementary data are available at JXB online. Table S1. Expression profiles and categories of strongly and moderately induced transcripts in response to photorespiratory stress Abbreviations Abbreviations ABA abscisic acid APX ascorbate peroxidase bZIP basic leucine zipper CRE cis-regulatory element CYP cytochrome P450 monooxygenase GPX glutathione peroxidase GSH glutathione GSSG glutathione disulfide GST glutathione S-transferase HSF heat shock factor HSP heat shock protein MAPK mitogen-activated protein kinase MV methyl viologen PRX peroxiredoxin PTM post-translational modification RBOH respiratory burst oxidase homolog RLK receptor-like kinase ROS reactive oxygen species SA salicylic acid TF transcription factor TRX thioredoxin UGT UDP-glycosyltransferase Acknowledgements The authors thank Dr Inge De Clercq and Patrick Willems for useful comments on gene expression data analysis, and Dr Martine De Cock for help editing the manuscript. 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Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Journal of Experimental BotanyOxford University Press

Published: Apr 5, 2018

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