Abstract
Hydrogen peroxide (H2O2) and nitric oxide (NO) are biological messengers that control a plethora of physiological functions integral to plant biology such as seed germination, growth, development, flowering, or plant response to stress. Furthermore, the interplay between the signaling pathways governed by these redox molecules has emerged as crucial during plant response to different stress situations. In recent years, to gain in the knowledge of the mode of action of these signaling molecules at molecular levels, different NO donors and H2O2 have been used in medium- and large-scale transcriptomic analyses including microarray, cDNA-amplification fragment length polymorphism (AFLP), and high-throughput sequencing (RNA-seq technology). Following this strategy, a high transcriptional reprogramming induced by both NO and H2O2 has been proposed. In this regard, thousands of NO- and H2O2-cell targets have been identified in different plant species and organs and predicted to be related to a wide diversity of biological processes. However, some authors have identified by comparing different transcriptomic analysis that there is a low overlap in the transcriptomic data available under different treatment conditions as well as different organ analyzed. In this sense, more transcriptomic data comparisons will help in the identification of the NO- and H2O2-specific targets and even the common genes involved in both H2O2- and NO-dependent signaling events.
In this book chapter, we will offer an update about the recent knowledge concerning the transcriptional regulation induced by NO and H2O2. With this purpose, the recent data from the different medium- and large-scale transcriptomic analyses have been discussed. In addition, it is also provided an overview about the interplay between H2O2- and NO-dependent signaling mechanism and the need to further identification of common targets during the coordinated response to different stress situations.
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1 Introduction
Redox molecules are essential components of the signaling mechanisms integral to plant biology. Among the most important redox molecules are reactive oxygen species (ROS) such as hydrogen peroxide (H2O2) and reactive nitrogen species (RNS) as nitric oxide (NO) and its derived molecules. ROS and RNS are a double-edge sword because at low concentrations they act as essential molecules involved in plant signaling processes, and at high concentrations they can alter cellular redox homeostasis and therefore being toxic and inducing cellular damages (Cerny et al. 2018). It is well established that during plant response to different stress situations, a burst of ROS and RNS takes place and therefore a nitro-oxidative stress is induced (Corpas and Barroso 2013). Under these conditions, ROS and RNS could act independently or coordinately in the regulation of signaling events leading to face the adverse situations. In this context, the interplay between both signaling pathways has emerged as crucial to regulate plant response to stress (Lindermayr and Durner 2015; Begara-Morales et al. 2016; Niu and Liao 2016; Lindermayr 2018). To transmit their bioactivity, these redox molecules act via posttranslational modifications that can regulate protein function and therefore being an essential part of signaling mechanisms (Astier and Lindermayr 2012; Cerny et al. 2018). In addition, as part of the signaling events governed by these redox molecules, a transcriptional regulation under these adverse conditions takes place to coordinate the plant response to stress. In the last decade, the development of the transcriptomic approaches, which use a part of a whole-genome analysis of different plant species, such as cDNA-amplification fragment length polymorphism (AFLP), microarray, and especially the high-throughput sequencing (RNA-seq technology), has facilitated the identification of thousands of H2O2- and NO-specific target genes under different physiological and stress situations (Ferrarini et al. 2008; Boscari et al. 2013; Begara-Morales et al. 2014b; Blaby et al. 2015; Li et al. 2017). Therefore, significant efforts have been made to unravel the transcriptional regulation mediated by these ROS and RNS that leads to a strong transcriptional reprogramming. However, most of these studies have been performed via the exogenous administration of H2O2 and different NO donors (Ferrarini et al. 2008; Boscari et al. 2013; Begara-Morales et al. 2014b; Blaby et al. 2015; Li et al. 2017). In this regard, further analyses to analyze the in vivo implication of these molecules during plant response to different stress conditions are required.
In this book chapter, we will explore the recent state-of-the-art knowledge concerning recent results obtained by a wide range of transcriptomic approaches to offer an overview of the understanding of H2O2- and NO-induced gene expression profile changes under different physiological and stress situations in plants. Due to the low overlap in the results obtained under different treatment conditions, plant species, or even NO donors (Ferrarini et al. 2008; Besson-Bard et al. 2009b; Blaby et al. 2015), the need to perform more comparisons of the transcriptomic data available to improve our knowledge in the H2O2- and NO-signaling events is also discussed.
2 Nitric Oxide Induces a High Transcriptional Reprogramming Under Physiological and Stress Conditions
Nitric oxide (NO) is a key biological messenger that governs a multitude of functions integral to plant biology (Mur et al. 2013). For instance, NO has been involved in seed germination (Albertos et al. 2015), flowering (He et al. 2014; Kumar et al. 2016), stomata closure (Wang et al. 2015), or plant response to stress (Yu et al. 2014; Fancy et al. 2016). It usually transmits its bioactivity through interaction with essential biomolecules such as proteins, nucleic acids, and fatty acids. In this regard, NO research has been traditionally focused on the regulation of protein function via posttranslational modifications (NO-PTMs) such as S-nitrosylation and tyrosine nitration (Astier and Lindermayr 2012) (Fig. 1). S-nitrosylation consists of the reversible addition of a NO group to a specific thiol group in a cysteine (Cys) residue leading to S-nitrosothiols (SNOs) formation (Hess et al. 2005). On the other hand, tyrosine nitration, which is usually mediated by peroxynitrite, is produced by the irreversible attachment of a NO2 radical to the aromatic ring of the tyrosine residue yielding 3-nitrotyrosine (Radi 2004) that is considered a nitrosative stress marker rather than a signaling process (Corpas et al. 2013). In last years, the development of new proteomic approaches has allow the identification of hundreds of proteins that are NO-PTM targets under different physiological and stress situations (Tanou et al. 2009; Hu et al. 2015). Consequently a wide range of cellular processes have been proposed to be regulated by these NO-PTMs.
Otherwise, gene expression changes are also part of NO-dependent signaling events (Fig. 1). One of the first evidence showing the NO-dependent induction of defense gene was carried out in tobacco plants and tobacco suspension cells. In this study, recombinant nitric oxide synthase (NOS) from mammals and NO donors as S-nitrosoglutathione (GSNO), and S-nitroso-N-acetyl-DL-penicillamine (SNAP), induced the expression of defense-related genes such as pathogenesis-related 1 protein (PR1) and phenylalanine ammonia lyase (PAL) (Durner et al. 1998). From this initial work, the development of the omic technologies has allowed to analyze the effect of NO on transcriptional regulation using a large part or the whole-genome (Badri et al. 2008; Ferrarini et al. 2008; Palmieri et al. 2008; Ahlfors et al. 2009; Begara-Morales et al. 2014b). Therefore, these technologies permit to have a general perspective of the NO-dependent signaling in a single experiment. In the following sections, we will analyze the most recent and relevant data concerning the NO-dependent transcriptional reprogramming obtained by different technology approaches.
2.1 Nitric Oxide-Responsive Genes Identified by cDNA-Amplification Fragment Length Polymorphism (cDNA-AFLP) and Microarray Analysis
The transcriptomic technologies have allowed significant advances in understanding the molecular basis of NO action. Most of these studies have been carried out under plant response to pathogen attack and/or using different NO donors (Badri et al. 2008; Ferrarini et al. 2008; Ahlfors et al. 2009; Begara-Morales et al. 2014b). First studies were conducted using a microarray analysis in which a cDNA microarray containing 200 defense-related genes and 50 genes related to primary metabolism was employed to determine gene expression changes in Arabidopsis suspension cells treated with the NO donor NOR-3 ((E)-ethyl-2-[(E)-hydroxyimino]-5-nitro-3-hexeneamide) (Huang et al. 2002). Following this approach, pathogenesis-related (PR) and antioxidant genes such as peroxidases and glutathione S-transferases were proposed to be modulated by NO. Interestingly, cytochrome c respiration was inhibited by NO, whereas one of the NO-induced genes was alternative oxidase 1a (AOX1a) that resulted in an increased respiration via the alternative pathway. Furthermore, NO-induced AOX was independent of salicylic acid (SA), suggesting that it may participate to counteract the toxicity of NO and therefore having an essential function for cellular homeostasis under NO stress (Huang et al. 2002). Moreover, Arabidopsis gene expression profile was analyzed by cDNA-amplification fragment length polymorphism (AFLP) transcript profiling after leaves infiltration with the NO donor sodium nitroprusside (SNP) (Polverari et al. 2003). Following this approach, it was observed the modulation of 120 genes among the 2500 cDNA examined. The NO-responsive genes were mainly related to signal transduction, disease resistance and cell death, ROS-related and stress response, photosynthesis, cellular transport, and basic metabolism (Polverari et al. 2003). Interestingly, most of NO-modulated genes identified were previously proposed to be regulated in other stress-related experiments, especially in disease-related conditions according to public microarray analysis data (Polverari et al. 2003). These results, pointing toward the NO-responsive genes have a crucial role during plant response to stress. Subsequently, it was shown that lipopolysaccharides (LPS) induced a rapid burst of NO with a concomitant regulation of gene expression, suggesting a functional link between the production of NO and gene induction by LPS (Zeidler et al. 2004). Moreover, a custom-designed cDNA microarray containing about 700 defense-related genes, which encodes PR proteins or protein induced by pathogens and abiotic stresses, was used to analyze gene expression changes caused by LPS and linked to a functional regulation of these genes by NO (Zeidler et al. 2004). In this context, the cDNA microarray analysis identified different defense or stress-associated genes including glutathione S-transferases, cytochrome P450, and different PR proteins, altogether contributing to the activation of plant defense responses (Zeidler et al. 2004). Besides these custom-designed arrays containing mainly genes related to defense, different genome-scale analyses have been performed too deep in the knowledge of the transcriptional reprogramming after perception of the NO signal by the cell. In this sense, stress-related genes were also proposed to be modulated by NO in Arabidopsis thaliana using SNP as NO donor (Parani et al. 2004). The advantage of this study was to use the whole-genome ATH1 microarray, allowing analyzing over 24,000 genes. After Arabidopsis irrigation with SNP and 2-[4-carboxyphenyl]-4,4,5,5-tetramethylimidazoline-1-oxy-3-oxide (cPTIO) as NO scavenger, 342 upregulated and 80 downregulated genes in response to NO were identified. Most of these genes were proposed to be involved in plant defense response such as some genes containing leucine-rich repeats (NBS-LRRs), non-race-specific disease resistance gene (NDR1), and different proteins related to disease resistance. Among these defense-related genes highlight some transcription factors with important functions during plant response to disease such as some members of the WRKY and ethylene-responsive element-binding (ERBP) transcription factor families. In this regard, about 10% of the NO-responsive genes were identified as transcription factors, suggesting the strong effect of NO on modulating gene expression profile. Moreover, genes related to protection against oxidative stress, iron homeostasis, or signal transduction including different kinases were identified as regulated by NO (Parani et al. 2004). In addition, NO treatment triggered the expression of transcripts encoding for dehydration-responsive element-binding proteins (DREB1 and DREB2) and late embryogenesis abundant (LEA) proteins that could confer drought, cold, and salinity tolerance in plants (Parani et al. 2004). Moreover, another microarray containing 26,090 genes and therefore covering almost the whole-genome in Arabidopsis was employed to identify NO targets in Arabidopsis roots (Badri et al. 2008). With this purpose, Arabidopsis plants were treated with 250 μM of SNP, and roots and root exudates were analyzed 3 and 6 h posttreatment. As a result, 87 genes differentially expressed with a fold change more than twofold were identified after NO treatment. It is interesting to note that following NO treatment there are a high number of repressed genes and few induces genes. In this analysis, different transport systems probably related to root exudation such as MATE, ABC, or MFS transporters appear to be modulated by NO treatment. In addition, different genes involved in defense signaling, antimicrobial activities, and regulation of cellular redox state were also identified to be modulated by NO in roots (Badri et al. 2008). Interestingly, in parallel to the identification of NO-responsive genes, in this work the effect of other signaling compounds such as methyl jasmonate (MetJA) and salicylic acid (SA) on gene expression changes was also analyzed. The processes affected by these elicitors are similar to those identified in NO treatment, but the set of genes regulated by each compound were different, suggesting that these signaling molecules act through different signaling mechanisms. In this regard, the results of this study only identified the NAC3, a member of NAC transcription factor family, as regulated by the three signaling compounds analyzed (Badri et al. 2008).
Another dedicated microarray was constructed to analyze the behavior of NO-responsive genes during pathogenic and symbiotic interactions in Medicago truncatula plants (Ferrarini et al. 2008). First, roots from 4-week-old plants were treated with SNP or GSNO as NO donors, and a cDNA-AFLP analysis with an estimated coverage of 55% of the Medicago truncatula transcriptome was performed. In this way, 1023 cDNA fragments were differentially regulated by these NO donors. These fragments that corresponded to 999 NO-responsive genes were then employed to construct the dedicated MtNO array (Ferrarini et al. 2008). This MtNO was first used to analyze GSNO and SNP-responsive genes to identify if these NO donors modulate a common set of genes. Surprisingly, GSNO and SNP exerted the same regulatory effects on only 11% of genes in leaves and 1.6% in roots, and there was a coincident between roots and leaves of only 1.6% of the differentially expressed genes. These results suggest that the NO-dependent modulation of gene expression could be dependent on the NO donor and it also could be organ-specific (Ferrarini et al. 2008), as lately confirmed (Begara-Morales et al. 2014b). Subsequently, this MtNO array was employed to monitor the modulation of these NO-responsive genes during the incompatible and symbiotic interactions. During the incompatible infection of M. truncatula with C. trifolii, there was a modulation of 275 NO-responsive genes mainly related to defense signaling, ROS metabolism, lipid signaling pathways, proteasome degradation, and different genes related to signal transduction such as kinases, phosphatases, and different transcription factors. On the other hand, the symbiotic interaction regulated the expression of 290 out of the 999 NO-responsive genes in the MtNO array. These genes were proposed to be mainly related to flavonoid biosynthesis, redox signaling, and primary metabolism. After transcriptomic data analysis, the authors suggest that NO could have an essential role during symbiotic nodule development and functioning (Ferrarini et al. 2008) as it was subsequently demonstrated (Puppo et al. 2013; Damiani et al. 2016). SNP was also used as NO donor in another microarray assay leading to identify NO targets and its relation with ozone-induced cell death in Arabidopsis thaliana (Ahlfors et al. 2009). Using a full genome array in leaves sprayed with 0.5 mM SNP for 3 h, 614 NO-responsive genes (579 upregulated and 35 downregulated) were identified, which were mostly related to various abiotic and biotic stresses or hormone metabolism. In addition, the treatment of Arabidopsis leaves with ozone (O3) showed about an 80% of similarity in the expression profile to NO, with only three genes that are modulated in an opposite manner by these compounds. Interestingly, the combination of NO and O3 had a significant effect on hormone concentrations, occurring a large increase in JA hormone. In addition, the authors showed that the combined treatments of O3 and SNP or SNAP produced the attenuation of SA and ethylene-related genes and therefore NO could be involved in the induction and regulation of the O3-induced cell death (Ahlfors et al. 2009).
In an elegant work, cadmium (Cd2+) was proposed to induce NOS-like-mediated NO production in Arabidopsis roots and leaves, with NO having a role in Cd2+-induced root growth inhibition (Besson-Bard et al. 2009a). To identify the root genes regulated by NO during Cd2+ treatment, a genome-scale array covering 22,089 nuclear genes was used. Thus, plants were exposed to 30 μM Cd2+ and/or L-NAME, a NOS animal inhibitor, and those genes whose modulation by Cd2+ was modified or completely abolished by L-NAME were selected as NO targets. In this way, 783 genes were identified as Cd2+-responsive genes and 43 of them were also NO-dependent genes. These NO-modulated genes appear to be related to iron homeostasis, proteolysis, nitrogen assimilation and metabolism and root growth. Interestingly, the authors conclude that NO contributes to Cd2+ toxicity by favoring Cd2+ versus Ca2+ uptake and by initiating a cellular pathway resembling those activated upon iron deprivation (Besson-Bard et al. 2009a). In the same work, plants treated with 4 mM of L-NAME for 24 h provide a valuable information on genes whose expression could be modulated by a NOS-like activity sensitive to L-NAME (Besson-Bard et al. 2009a, b). In this regard, L-NAME produced expression changes in 2656 genes, among which the L-NAME-repressed genes are mainly related to primary and secondary metabolism, abiotic and biotic stress, and transport of micronutrients ions, ions, and carbohydrates. Interestingly, L-NAME produced the repression of genes related to auxin metabolism and transport (Besson-Bard et al. 2009b).
A microarray analysis was also performed to analyze the effect of NO on root architecture in sunflower plants (Monzón et al. 2014). In this context, NO donors produced a reduction in the primary root length without effect on the lateral root development, whereas cPTIO induced a general change in the root architecture mainly affecting the number of the lateral roots. Therefore, a Sunflower Custom Oligo Microarray containing 41,013 genes was used to characterize those genes specifically affected by cPTIO. Following this approach, 330 genes regulated by cPTIO were identified in sunflower roots. These genes are peroxidases, cytochrome P450, glutathione reductases, and different transmembrane transports among other genes differentially expressed. Interestingly, NO depletion caused the regulation of an important set of genes related to secondary metabolism, especially phenylpropanoid biosynthesis and particularly lignin biosynthesis. These results suggest that NO is crucial for regulating root architecture and lignin composition and therefore for plant growth and development (Monzón et al. 2014).
Using a cDNA-AFLP analysis, senescence-related genes were identified in Medicago truncatula plants (De Michele et al. 2009). Interestingly, this data collection was compared to previously reported NO-responsive genes in the same plant species (Ferrarini et al. 2008) obtaining about 50 genes being modulated in both senescence and NO treatments (De Michele et al. 2009). Interestingly, taking into account the high proportion of regulative genes expressed in both conditions, the authors suggested that there are conserved mechanisms in the onset and execution of the plant cell death events (De Michele et al. 2009) as previously pointed by other study (Quirino et al. 1999).
2.2 Nitric Oxide-Induced Transcriptional Regulation Determined by RNA-seq Analysis
Apart from the cDNA-AFLP and microarray analysis, in the last decade, new massively parallel sequencing or RNA-seq has emerged as a useful tool that could replace and improve existing methods because of their advantages over array-based methods (Wilhelm and Landry 2009), highlighting it is not necessary to have previous knowledge of the transcribed regions and allow gene expression quantification in a single experiment (Wilhelm and Landry 2009). Consequently, this RNA-seq technology has been used to deep in the knowledge of the NO-signaling events under physiological and stress situations. In this regard, Illumina RNA-seq technology was employed to analyze the dynamic changes in gene expression at two different stages of the symbiotic interaction of Medicago truncatula with S. meliloti: early organogenesis of the nodules and fully differentiated and functioning nodules (Boscari et al. 2013). This approach allowed identifying 1670 new genes and 7595 new transcribed regions in M. truncatula. In addition, about 35% of the genes identified by RNA-seq to have differential regulation during nodulation were not present on the Affymetrix Medicago GeneChip. These results confirm that RNA-seq appears to have a higher sensitivity and ability to discover new genes than microarrays approaches (Boscari et al. 2013). An important point in this work was the analysis of NO function in the nodulation transcriptome. With this purpose, a RNA-seq analysis was performed on inoculated roots treated with cPTIO as a NO scavenger (Boscari et al. 2013). Removing NO caused differential expression of 2030 genes, and surprisingly, NO produced a downregulation in the number of reads identified, suggesting a potential role of NO in decreasing transcriptome complexity during nodulation. Interestingly, under NO depletion there are a high number of downregulated transcriptional regulators related to defense reactions. Consequently, it is suggested that NO plays a crucial role repressing the defense system during early nodulation and therefore favoring the plant-microbe interaction that takes place during the establishment of the symbiotic interaction. By contrast, during a pathogenic interaction, NO usually induces the expression of defense genes (Boscari et al. 2013). Another Illumina RNA-seq analysis was performed too deep in the knowledge of the resistance of the wheat variant Wangshuibai to the Fusarium head blight (FHB) disease in comparison to the susceptible mutant NAUH117 (Xiao et al. 2013). Among all the gene expression changes, some ROS and NO producing and removing systems were induced in the susceptible NAUH11 while were repressed or remained stable in the resistant variant Wangshuibai. Among these ROS and NO-related genes are NADPH oxidases, ascorbate peroxidase, glutathione peroxidase, superoxide dismutase, catalase, or peroxiredoxin. Consequently, authors suggested that ROS/NO could contribute to the necrotrophic phase during the infection and therefore the downregulation of these reactive species would allow to enhance the resistance to FHB in wheat plants (Xiao et al. 2013).
Besides these transcriptional reprogramming analyses upon pathogen infection, most of the transcriptional analyses using RNA-seq have been performed using NO donors. For instance, dynamic changes in gene expression profile have been analyzed in birch cells (Betula platyphylla) after treatment with SNP for 12 h using Solexa sequencing (Zeng et al. 2014). In this way, 403 upregulated and 971 downregulated genes were identified after application of the exogenous SNP. An important set of these NO-responsive genes are involved in protection against ROS, probably as a consequence of the induction of O2 ·− production after SNP treatment. Consequently, it is not surprising that within the NO-regulated genes in birch cells, there were 30 upregulated genes encoding proteins with antioxidant functions such as glutathione S-transferases, thioredoxin peroxidase, superoxide dismutases, or ascorbate peroxidase. In addition, different processes integral to plant biology were identified as target of NO as carbohydrate metabolism and cell wall biosynthesis, terpenoid biosynthesis, or growth regulation (Zeng et al. 2014).
GSNO has been also used to analyze the transcriptional changes in Arabidopsis plants under nonstress conditions (Begara-Morales et al. 2014b). GSNO was exogenously applied by roots for 3 h, and an Illumina RNA-seq was carried out in leaves and roots of Arabidopsis plants given as a result the identification of 3263 GSNO-responsive genes in the whole plant. Overall, GSNO provokes expression changes of an important set of stress-related genes suggesting that GSNO is perceived as a molecular cue to trigger NO-downstream signaling events leading to protect against a stress situation (Begara-Morales et al. 2018). In this context, different PR genes, defense-related transcription factors, or genes involved in wounding response have been proposed to be modulated by GSNO. In addition, in leaves of Arabidopsis, there was an important induction of a member of methionine sulfoxide reductase B (MSRB) family, concretely MSRB7 which is related to the protection against oxidative damages via regeneration of methionine from oxidized methionine. Interestingly, GSNO also induced proteins related to methionine degradation, suggesting a potential role of NO in methionine metabolism as previously reported in E. coli (Flatley et al. 2005). However, the most interesting analysis using this transcriptomic data was to determine those genes differentially expressed in leaves and roots and especially those genes with an organ-specific modulation. In this regard, leaves-specific NO-responsive genes were related to plant response to stress processes, whereas root-specific genes were related to developmental processes. These results confirm that NO can regulate a different set of genes depending on the tissue analyzed and therefore conferring to NO the capacity to modulate gene expression in an organ-specific manner (Begara-Morales et al. 2014b) as previously suggested by other transcriptomic analyses (Ferrarini et al. 2008).
The involvement of NO in the flowering process in Oncidium plants has been recently analyzed by Solexa transcriptomic analysis (Kumar et al. 2016). After transcriptomic data analysis, differentially expressed genes related to NO metabolism such as nitrate and nitrite reductases were identified in flowering. In addition, a significant reduction of nitrate reductase activity and NO level was observed during this process, suggesting a key role of NO in the transition phase and flowering process. Furthermore, exogenously applied SNP on ascorbate Arabidopsis-deficient mutants induced a downregulation of flowering-associated genes and the concomitant delay in flowering, suggesting an essential role of NO signaling in flowering repression (Kumar et al. 2016).
NO has been previously proposed to govern a multitude of physiological and stress response in plants as we can deduce for the transcriptomic analysis aforementioned. Following with this line, the infiltration of Arabidopsis leaves with 1 mM S-nitrosocysteine (Cys-NO), a potent NO donor, for 6 h and the subsequent RNA-seq analysis allowed to identify 1165 differentially expressed genes, with 463 upregulated and 702 downregulated. These Cys-NO-responsive genes were involved in a wide range of plant processes such as biotic and abiotic stress, hormone metabolism, or secondary metabolism among others (Hussain et al. 2016). It is interesting to note that 604 out of 1165 of these CysNO-responsive genes encode transcription factors (TFs), that in turn regulate a wide range of processes integral to plant biology (Hussain et al. 2016). The experimental analysis of the role of NO regulating these TFs could open new lines of research in the field by exploring the role of NO as a regulator of the processes in which these TFs are involved. Indeed, a new RNA-seq analysis following Arabidopsis leaves infiltration with 1 mM Cys-NO was focused on those genes with transcriptional activity (Imran et al. 2018). A total of 673 differentially expressed TFs with important function on a wide range of biological processes were identified. Three of these TFs, DDF1, RAP2.6, and AtMYB48, were randomly selected, and their functional implications were analyzed. In this regard, it was demonstrated that these genes act as key regulators of plant growth and immunity. Defective mutants of DDF1 and RAP2.6 compromised basal and effector triggered immunity, suggesting a vital role of these TFs in regulating these plant defense systems (Imran et al. 2018).
The involvement of NO as modulator of plant response to arsenic stress was also analyzed by a massive sequencing RNA analysis (Singh et al. 2017). With this purpose, rice plants were subjected to arsenic stress alone or combined with SNP at different time points, and an Illumina RNA-seq transcriptomic analysis was performed. Following the bioinformatic analysis, NO was proposed to regulate different metal transporters, stress-related genes, hormones, and secondary metabolism genes that together could be involved in the arsenic detoxification processes. Therefore, authors conclude that NO reduces arsenic toxicity by modulating regulatory networks involved in arsenic detoxification (Singh et al. 2017).
Similar biological processes to those described in the aforementioned transcriptomic analysis have been identified to be modulated by NO following RNA-seq analysis in upland cotton (Gossypium hirsutum) treated with SNP for 3 h (Huang et al. 2018). Interestingly, the authors performed a comparison of different NO-mediated transcriptomic reprogramming in different plant species and different NO donors. This comparison highlights that there is a low overlap between different NO donors and tissue analyzed, confirming that the NO effect could depend on the source of NO and also have an organ-specific mode of action. Furthermore, the results could depend on the transcriptomic sequencing strategy perform (Huang et al. 2018), with RNA-seq being a more sensitive approach.
Very recently, the occurrence of nitro-fatty acids (NO2-FAs) has been described in plants for the first time (Mata-Pérez et al. 2016b). Interestingly, the nitro-linolenic acid (NO2-Ln) has been proposed to have an essential role during development and stress response in Arabidopsis plants (Mata-Pérez et al. 2016b). In this context, NO2-Ln appears to have an essential role in the early stages of development as the greater levels have been detected in seeds with the subsequent decrease throughout the plant development. Furthermore, different abiotic stress situations such as salinity, cadmium exposure, or wounding are able to increase NO2-Ln levels suggesting a role of this signal molecule in plant response to abiotic stress. In addition, NO2-Ln has the capacity to act as a NO donor and therefore regulating the NO-mediated signaling (Mata-Pérez et al. 2016a). Too deep in the signaling mechanisms of this NO2-Ln and to analyze the transcriptional reprogramming that it could induce, an Illumina RNA-seq analysis was performed in Arabidopsis suspension cells treated with 10 and 100 μM NO2-Ln (Mata-Pérez et al. 2016b). The transcriptomic analysis revealed that NO2-Ln induced expression changes in 1308 genes, with 129 upregulated and 187 downregulated at least twofold. These NO2-Ln-responsive genes have been proposed to be mainly involved in plant response to abiotic and oxidative stress, mainly by activating heat shock proteins and supporting a conserved signaling mechanism in both animals and plants during the defense response (Kansanen et al. 2009; Mata-Pérez et al. 2016b).
3 Transcriptional Regulation Mediated by Hydrogen Peroxide
Reactive oxygen species (ROS) are a family of reactive molecules composed of singlet oxygen (O2 1), hydrogen peroxide (H2O2), superoxide anion (O2 ·−), or hydroxyl radical (OH). It is widely recognized that H2O2 plays crucial roles in oxidative signaling (Foyer and Noctor 2016). This ROS can be synthesized from the reduction of molecular oxygen (O2), the chemical reduction or dismutation of superoxide or H2O2, a reaction that is accelerated by superoxide dismutases (SODs), as well as by a two-electron reduction of O2 through various oxidases such as glycolate oxidase (GOX) located in peroxisomes (Foyer and Noctor 2016; Cerny et al. 2018). H2O2 is involved in different developmental and physiological processes such as seed germination, programmed cell death, senescence, flowering, or stomatal closure (Niu and Liao 2016). In addition, it is also a signaling molecule involved in plant response to different stresses such as drought, salt, extreme temperatures, or heavy metal (Niu and Liao 2016). H2O2 transmits its action through different PTMs that are produced by oxidation of different amino acid such as cysteine and methionine (Niu and Liao 2016; Cerny et al. 2018). Cysteine residue is very sensitive to oxidation, showing different oxidation states depending on the cellular redox state that induce different PTMs related to signaling or degradation processes (Fig. 1). These PTMs have been proposed to have important functions in the regulation of different physiological and stress response in plants (Cerny et al. 2018). Besides PTMs, H2O2 is also able to modulate gene expression changes as part of its function as a signaling molecule (Fig. 1). In this regard, an interplay between H2O2 and SA has been proposed to control the expression of defense genes (Herrera-Vásquez et al. 2015). In addition, H2O2 was proposed to act as a second messenger after wounding stress in tomato plants (Orozco-Cárdenas et al. 2001). In this context, H2O2 appears to be involved in a cascade of intracellular events in which jasmonate activates the signaling genes (early genes), whereas H2O2 could act as a second messenger activating the defense genes (late genes) in response to wounding stress. Due to its low stability and the presence of H2O2 scavengers, it has been questioned its function as a long-distance molecule (Cerny et al. 2018). Keeping this in mind, the detection and use of H2O2 are not always straightforward tasks, so that catalase-deficient mutants, impaired in one of the major H2O2 scavenger, have been employed to analyze the effect of the sustained H2O2 stress over time. These mutants appear to produce a disruption of the redox state and peroxisome function, and therefore they are more sensitive to different abiotic stresses (Vandenabeele et al. 2004; Su et al. 2018). To analyze the H2O2−signaling events, different cDNA-AFLP and microarray analysis have been performed. In this regard, using a catalase-deficient tobacco plant exposed to high light, the effect of H2O2 accumulation on gene expression profile was analyzed by cDNA-AFLP (Vandenabeele et al. 2003). 713 differentially expressed genes were detected and predicted to be mainly involved in plant response to stress, proteolysis, mitochondrial metabolism, or cell death among other biological processes (Vandenabeele et al. 2003). In the same line, a microarray composed of 6008 cDNA from Arabidopsis was employed to analyze the effect of the accumulated H2O2 in catalase-deficient mutants exposed to high light stress for 3, 8, and 23 h (Vandenabeele et al. 2004). The main functional categories regulated by H2O2 were related to development, interaction with the environment, defense, cellular communication, and signal transduction or cellular transports, among others. Catalase-deficient mutants also induced the expression of nuclear genes under nonstress conditions, and these effects were amplified by high light stress (Vanderauwera et al. 2005). In this case, it was shown that H2O2 plays an essential role during high light stress through the transcriptional activation of the small heat shock proteins. Interestingly, the heat shock transcription factors were proposed to act as sensor of hydrogen peroxide under different stresses that induce an oxidative stress (Miller and Mittler 2006), with a significant H2O2-mediated upregulation of the heat shock proteins taking place in peroxisomes (Sewelam et al. 2016). In addition, an impairment in the anthocyanin biosynthesis pathway was identified and proposed to be responsible for the more sensitive phenotype of catalase-deficient mutants to abiotic stress (Vanderauwera et al. 2005). Taking together, these results show a high reprogramming of the transcriptome by H2O2. Moreover, the establishment of Medicago truncatula-Sinorhizobium meliloti symbiosis is also regulated by H2O2. The use of DPI as a NADPH oxidase inhibitor, which reduces ROS and specially H2O2 production, was used to determine the function of ROS on this symbiotic interaction (Andrio et al. 2013). By microarray analysis, 447 differentially expressed genes were identified after bacterial inoculation. Of these genes, 301 were also affected by DPI treatment in inoculated roots, suggesting a crucial role of ROS in the transcriptomic regulation during this symbiotic condition. Within this group of genes, potentially regulated by ROS after bacterial inoculation, is the gene MtSpk1 that encodes a putative protein kinase whose deficiency impairs the establishment of the symbiotic interaction (Andrio et al. 2013). The role of H2O2 during plant-pathogen interaction was also demonstrated in grapevines plants infected with Flavescence dorée (FD), one of the most severe phytoplasma diseases affecting these plants (Gambino et al. 2013). In this work, the phenomenon of recovery after pathogen infection was investigated. In this line, infected plants exhibited a decrease in H2O2 levels probably due to an upregulation of the H2O2 scavenger systems compared to healthy and recovery plants. Interestingly, recovery plants showed an upregulation of genes involved in H2O2 production, whereas most of the scavenger systems were not affected, leading to an accumulation of H2O2. Following expression analysis of different defense genes, the recovery phenomenon was proposed to be mediated by the activation of ethylene biosynthesis and defense genes probably in a SA-independent manner (Gambino et al. 2013).
In an interesting work, glycolate oxidase overexpressing mutants associated with increased levels of H2O2 in chloroplasts and catalase-deficient mutants that accumulate H2O2 in peroxisomes were used to test if H2O2-mediated transcriptional changes have a subcellular localization specificity (Sewelam et al. 2016). These mutants were grown under normal conditions and then transferred to photorespiratory conditions to increase H2O2 production in both organelles. Following a microarray analysis, a set of differentially expressed genes were identified as peroxisome or chloroplast specific as well as genes with a response independent from the subcellular localization. Interestingly, the results showed that H2O2 from chloroplast modulate the expression of transcription factors, protein/receptor kinases, or defense genes, whereas H2O2 from peroxisomes are mainly involved in cell repair responses (Sewelam et al. 2016).
Besides microarray approaches, a few RNA-seq analyses focused on the unrevealing H2O2-induced signaling events have been performed. However, less transcriptomic analysis based on the RNA-seq technology is available in comparison to NO. In this context, a RNA-seq analysis showed that cat1/2/3-deficient triple mutant induced the differential expression of 2852 genes compared to wild-type, including 241 transcription factors that appear to be crucial in the perception and signaling events related to H2O2 in eukaryotes (Marinho et al. 2014; Su et al. 2018). Interestingly, 1972 differentially expressed genes were also identified in comparison to cat1/2 double mutant (Su et al. 2018). As a general conclusion, authors propose that the differentially expressed genes are mainly involved in plant growth regulation and stress response processes. Furthermore, they suggest that the H2O2 produced in peroxisomes could serve as a peroxisomal retrograde signal with important functions in plant development (Su et al. 2018). The exogenous application of 1 mM H2O2 for 0.5 and 1 h to cell cultures of Chlamydomonas reinhardtii induced expression changes in 1278 genes, with the upregulation of transcripts mainly related to protein degradation, ROS detoxification, and stress response, whereas downregulated genes are involved in photosynthesis and central carbon metabolism, suggesting a crucial role of H2O2 in the regulation of these physiological processes (Blaby et al. 2015). After comparison of the transcriptomic results with previous public data, a significant overlap in the number of transcripts upregulated by H2O2 and singlet oxygen was detected. Interestingly, it was determined that the response of the heat shock proteins was specific to H2O2, supporting the idea that these proteins can act as sensors of H2O2 as mentioned above (Miller and Mittler 2006; Blaby et al. 2015). H2O2 is also involved in the adventitious roots formation in mung bean (Li et al. 2017). The treatment of mung bean plants after removing the hypocotyl basis with 10 mM H2O2 for 6 h induced a high transcriptional activity, whereas 24 h posttreatment a reduction in gene expression levels was observed. In this regard, after 6 h of treatment, the number of differentially expressed genes was 29.9% higher than in 24 h posttreatment. Overall, the most responsive genes were related to stress response, cell redox homeostasis, oxidative responses, cell modification, or hormone metabolism among others. Interestingly, after comparison of 6 h, 6–24 h, and 24 h posttreatment, two differentiate phases were identified in the adventitious roots formation, the induction, and the initiation stages. In this regard, protein degradation, cellular respiration, lipid transport, photosynthesis, flavonoid synthesis, and phenylalanine metabolism are among the biological processes proposed to be modulated by H2O2 during the induction stage. However, amino acids synthesis, transmembrane transporters, cell wall organization, protein synthesis, lipid metabolism, cytokinin-related pathway, and phenylpropanoid biosynthesis were more represented in the initiation stage. Interestingly, once again the upregulation of the heat shock proteins and heat shock transcription factors suggests their function as sensors of H2O2 (Li et al. 2017).
4 Interplay Between Hydrogen Peroxide and Nitric Oxide Signaling Events
Hydrogen peroxide (H2O2) and nitric oxide (NO) are considered secondary messengers involved in a plethora of processes integral to plant biology, ranging from seed germination and plant development to plant response to different stress situations (Niu and Liao 2016). It is well established that under different stress situations, a rapid burst of ROS and RNS is produced to mediate signaling events leading to cope these adverse situations. In this context, a growing number of evidences show that NO and H2O2 are produced under similar stress conditions and with similar kinetics, suggesting that the interplay between these two signaling molecules could have important functions in the modulation of the signaling events that ultimately coordinate plant defense (Niu and Liao 2016). Niu and Liao (2016) have reviewed the interaction of these signaling pathways during plant development and stress response. In this sense, the interplay between H2O2 and NO appears to be crucial in physiological processes such as cell death, senescence, root growth, pollen tube growth, and stomatal movement. In addition, this cross talk is also produced during plant response to different abiotic stresses such as drought, salt, extreme temperatures, or heavy metals (Niu and Liao 2016).
The first evidence of H2O2 and NO cross talk was evidenced during the hypersensitive cell death response in soybean cell cultures (Delledonne et al. 1998). It was shown that not only ROS but also NO is necessary for the hypersensitive cell death response, concluding that NO and ROS are complementary and could trigger a synergistic induction of this process (Delledonne et al. 1998). Subsequently, it was demonstrated that a balanced production of NO and ROS is necessary to trigger this response, where the interaction of NO with H2O2 plays a crucial role (Delledonne et al. 2001). In addition, a connection between NO and ROS pathways under different physiological and stress conditions has been widely reviewed (Corpas et al. 2011; Gross et al. 2013; Procházková et al. 2014). This interplay can be produced by regulation of specific enzymes involved in ROS metabolism by NO or by a connection in the transcriptional regulation induced by both signaling pathways. Regarding NO-PTMs, S-nitrosylation can modulate ROS metabolism through the regulation of the ROS producers and scavengers systems such as NADPH oxidase (Yun et al. 2011), catalase (Ortega-Galisteo et al. 2012), peroxiredoxin IIE (Romero-Puertas et al. 2007), and peroxiredoxin IIF (Camejo et al. 2015). In addition, the function of the main antioxidant systems has been proposed to be modulated by NO-PTMs, highlighting the regulation of the ascorbate-glutathione (Asa-GSH) cycle by NO (Begara-Morales et al. 2016). Interestingly, the modulation of ascorbate peroxidase (APX) by NO has emerged as a crucial point during plant response to abiotic stress (Lindermayr and Durner 2015). In fact, APX activity exhibits a dual regulation by NO-PTMs, being enhanced by S-nitrosylation and inhibited by tyrosine nitration (Begara-Morales et al. 2014a). In this regard, the Cys-32 in APX has been identified as a crucial amino acid regulated by S-nitrosylation during plant response to abiotic and oxidative stresses (Begara-Morales et al. 2014a; Yang et al. 2015). S-nitrosoglutathione reductase (GSNOR) enzyme degrades GSNO and indirectly controls total SNO levels in cells (Liu et al. 2001; Feechan et al. 2005). This enzyme has been proposed to play a crucial role in the regulation of SNO levels during plant development and response to a wide range of stresses (Begara-Morales and Loake 2016). Very recently, it has been proposed that GSNOR also plays a crucial role during cross talk between ROS and NO in plants (Lindermayr 2018). In this sense, in vitro H2O2 treatment and in vivo paraquat-induced oxidative stress inhibit GSNOR activity with the concomitant increase in SNO and GSH levels (Kovacs et al. 2016). In addition, it was shown that in GSNOR-deficient mutants, there is an increase in the transcriptional activation of redox-regulated genes and antioxidant enzymes, suggesting that oxidation of GSNOR could be crucial in the antioxidant response to cope the oxidative damage during abiotic stress (Kovacs et al. 2016).
The interplay at transcriptional level of these signaling pathways has been also suggested. In this regard, the cross talk between NO and ROS appears to be also crucial during the legume-Rhizobium symbiotic interaction (Puppo et al. 2013; Damiani et al. 2016). H2O2 has been proposed to regulate the infection process and bacterial differentiation into the symbiotic form and NO as important for the establishment of the symbiosis (Puppo et al. 2013). The transcriptomic data available also point toward a crucial regulation of Medicago truncatula-Sinorhizobium meliloti symbiosis by NO and H2O2 (Andrio et al. 2013; Boscari et al. 2013; Ferrarini et al. 2008). The comparison of these differentially expressed genes during symbiosis process as consequence of NO and H2O2 will allow identifying the common genes regulated by both signaling molecules. On the other hand, the transcriptomic data available highlight a high response of heat shock proteins and heat shock transcription factors to H2O2. In this regard, these transcription factors were proposed to act as sensor of hydrogen peroxide signal during plant response to stress (Miller and Mittler 2006). These transcription factors have been also recently shown to be transcriptionally activated by nitro-linolenic acid, which can act as a NO donor (Mata-Pérez et al. 2016a, b). These results suggest another point of interaction between H2O2 and NO that needs further investigations.
5 Conclusions and Future Perspectives
ROS and RNS encompass a set of redox molecules with an essential role in the cellular redox homeostasis, acting as crucial regulators of signaling events that coordinate fundamental processes integral to plant biology. In this regard, the interplay between ROS and RNS signaling pathways, especially H2O2 and NO, appears to be essential during plant response to a wide range of stress conditions. These signal molecules usually transmit their function via posttranslational modifications and regulation of the transcriptional activity in cells. Due to the wide range of processes and diverse functions that can be regulated by these signal molecules, it is more informative to analyze their function using different “omics” approaches such as large-scale proteomics or gene expression studies to better understand the signaling network in which they are involved. In this book chapter, we have analyzed recent data concerning the transcriptional reprogramming mediated by H2O2 and NO. These approaches have provided a huge availability of data concerning the gene expression profile changes induced by H2O2 and NO that sometimes overwhelm researchers during its analysis. In addition, these studies have been performed using different biological systems (Arabidopsis thaliana, Medicago truncatula, Glycine max, etc.) at different developmental stages and organs (cell cultures, seedlings, leaves, roots, hypocotyls, etc.) and even using different NO and ROS donors (GSNO, SNP, NOR-3, H2O2, O2 1, etc.). Consequently, it is not a straightforward task to make effective comparisons of these studies to establish a real perspective of the molecular basis of H2O2 and NO mode of action. For example, in Medicago truncatula plants exposed to SNP and GSNO, it was shown that only 11% of genes in leaves and 1.6% in roots are common targets of these NO donors. This result suggests a specific modulation of the genes depending on the NO source (Ferrarini et al. 2008). In the same line, a recent comparison of the transcriptomic data available has also emphasized that even the same NO donor induces different responses depending on the time of exposure and concentration (Huang et al. 2018). In this regard, the results could also depend on the application mode of the donor and the technology used in the sequencing analysis. Something similar takes place when different concentration of H2O2 is used to induce the transcriptional response. In addition, an organ-specific regulation of NO target genes has been proposed in Arabidopsis and Medicago plants, highlighting the low percentage of coincidence in the common genes regulated by NO in these organs (Begara-Morales et al. 2014b; Ferrarini et al. 2008). In this regard, Besson-Bard et al. (2009b) performed a comparison of different medium- and large-scale transcriptional analyses available until 2009 to identify common NO-responsive genes. Although they showed that there was not a high overlap of NO targets identified in the different analysis, a high percentage of the NO-responsive genes are related to oxidative stress generated in response to different stress conditions, supporting the idea that NO acts as a signal molecule involved in the adaptive response to various plant stress situations (Besson-Bard et al. 2009b). All these results highlight the necessity of performing more transcriptional data comparisons to identify a reliable set of genes that are targets of NO or H2O2. In addition, due to the interplay between these two signaling molecules, a comparison between the transcriptomic data available on NO-responsive genes and H2O2-responsive genes would be a good starting point to identify those genes that are common to both signaling pathways and their potential effect on plant response to stress. Additionally, in spite of the high number of NO and H2O2 target genes identified, little is known concerning the molecular characterization of the effect of this regulation on gene or protein function. In this respect, the transcriptomic data could be complement with proteomic and protein structural analysis to definitively unravel the effect of NO and H2O2 on the whole-cell response to different stress situations. Finally, more information regarding promoter sequences having a crucial role during H2O2- and NO-mediated signaling events is required.
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Acknowledgments
JCBM wishes to thank the Ministry of Economy and Competitiveness (Spain) for postdoctoral research funding within the Juan de la Cierva-Incorporación program. The work in our lab is supported by the ERDF grants co-financed by the Ministry of Economy and Competitiveness (projects BIO2015-66390-P) and the Junta de Andalucía (group BIO286) in Spain.
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Begara-Morales, J.C., Chaki, M., Valderrama, R., Mata-Pérez, C., Padilla, M., Barroso, J.B. (2019). Transcriptional Regulation of Gene Expression Related to Hydrogen Peroxide (H2O2) and Nitric Oxide (NO). In: Gupta, D., Palma, J., Corpas, F. (eds) Nitric Oxide and Hydrogen Peroxide Signaling in Higher Plants. Springer, Cham. https://doi.org/10.1007/978-3-030-11129-8_4
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