Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants

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In the latter case, please turn on Javascript support in your web browser and reload this page. The natural environment of plants is composed of a complex set of abiotic stresses and their ability to respond to these stresses is highly flexible and finely balanced through the interaction between signaling molecules. In this review, we highlight the integrated action between reactive oxygen species ROS and reactive nitrogen species RNS , particularly nitric oxide NO , involved in the acclimation to different abiotic stresses. Under stressful conditions, the biosynthesis transport and the metabolism of ROS and NO influence plant response mechanisms.

The enzymes involved in ROS and NO synthesis and scavenging can be found in different cells compartments and their temporal and spatial locations are determinant for signaling mechanisms. The mechanisms of abiotic stresses response triggered by ROS and NO involve some general steps, as the enhancement of antioxidant systems, but also stress-specific mechanisms, according to the stress type drought, hypoxia, heavy metals, etc. These changes may alter the activity, stability, and interaction with other molecules or subcellular location of proteins, changing the entire cell dynamics and contributing to the maintenance of homeostasis.

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However, despite the recent advances about the roles of ROS and NO in signaling cascades, many challenges remain, and future studies focusing on the signaling of these molecules in planta are still necessary. Therefore, at the cellular level, plant responses to the environment are extremely complex and involve interactions and crosstalk with many molecular pathways. One of the first plant responses to the environment involves reactive oxygen species ROS and reactive nitrogen species RNS , which are key signaling molecules and regulate many different plant processes through the activation of secondary messengers, the induction of gene transcription and changes in enzyme activity Gaupels et al.

Reactive oxygen species is a generic term used to describe chemical species formed from the incomplete reduction of molecular oxygen. NO is a gaseous, small, reactive molecule that readily diffuses across the cells and interacts with different cellular compounds, including other radicals Correa-Aragunde et al. Due to their high reactivity and potential to damage cellular structures under conditions of redox imbalance, the generation of ROS and RNS in cells was originally considered to be a uniquely harmful and damaging process Demidchik, ; Lushchak, Nitric oxide and ROS are involved in and interact with each other in a wide range of cellular processes, which include response to abiotic stresses Joudoi et al.

Ebook Reactive Oxygen And Nitrogen Species Signaling And Communication In Plants

It is easy to see, therefore, that the changes triggered by these signaling molecules are highly variable according to the environmental context. Due to the high complexity of this process, there is still much that is unclear about the signaling mechanisms triggered by ROS and NO, the interaction of these molecules with each other and with other components of the signaling pathway, and the balance between production and elimination of reactive species by antioxidants. A growing number of studies have sought to answer these questions, and many advances have been made in the field.

Thus, considering the central role of these molecules in the response and adaptation of plants to changes in the environment, the present review aims to summarize the existing knowledge of the interactions between ROS and NO in the plant response to abiotic stress, focusing on the sources and production sites of these molecules, interactions with other signaling components and molecular aspects.

As a result, the concentration of these reactive species is suddenly elevated, which is necessary to trigger specific cellular responses. These responses include defense mechanisms to abiotic stresses, such as increased concentration and activity of antioxidant systems Shi et al.

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It has been observed, for example, that the transcriptional changes mediated by H 2 O 2 produced in the apoplasts are distinct from the gene expression responses triggered by H 2 O 2 produced in the chloroplasts Gadjev et al. Similarly, the NO generated from the plasma membrane is important in hypoxic conditions, whereas the NO generated from the chloroplasts and mitochondria is involved in the response to heavy metals Kumar and Trivedi, Several studies have shown that stressful conditions stimulate the expression and activity of NADPH oxidases, leading to an oxidative burst Jajic et al.

Other oxidases and peroxidases associated with the cell wall are also involved in the generation of ROS in the apoplast, although their involvement in the response to stressors is not well defined Das and Roychoudhury, In addition to promoting specific signaling events, which involve interactions with local signals, the RBOH-mediated oxidative burst of ROS production triggers the production of ROS in neighboring cells, initiating a long distance signaling event called a ROS wave. Each cell along the ROS wave activates their own RBOH proteins, generating a systemic wave of propagation of ROS production, which travels through the apoplast from the initial tissue to whole plants at rates of up to 8.

SAA enables all plant cells, not just those who first perceived the external stimulus, to alter their gene expression and metabolism in response to the stressor.

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Although the ROS wave is necessary for SAA, the response elicited is not always specific to the stress that initiated the signaling process, suggesting that the main function of the ROS wave is to prepare the plant for SAA and that other signals are required to mediate stress-specific SAA Gilroy et al. In addition to the apoplast, various cellular organelles, such as chloroplasts and mitochondria, also generate ROS. In fact, when illuminated, chloroplasts are important sources of ROS due to the intense electron transport during photosynthesis and the release of oxygen in PSII Gupta and Igamberdiev, In mitochondria, ROS production occurs when the transfer of electrons exceeds the capacity of the alternative oxidase and the cytochrome oxidase to eliminate excess electrons, resulting in their transfer to molecular oxygen, mainly from complexes I and III.

Another organelle involved in ROS synthesis in stressful conditions is the peroxisome. These different pools of ROS, produced in distinct compartments, communicate with each other in the cells to regulate the plant metabolism. It is believed, for example, that the signal generated by the oxidative burst in the apoplast is transduced to chloroplasts, where a second wave of ROS generation is initiated Shapiguzov et al. This has also been observed in other organelles, such as peroxisomes, where ROS accumulation can alter gene transcription Sandalio and Romero-Puertas, The maintenance of ROS levels also involves the participation of antioxidant mechanisms, which are associated with the elimination of these reactive species and can be divided into enzymatic and non-enzymatic mechanisms.

In combination with these enzymes, non-enzymatic antioxidants, such as glutathione, ascorbate, and tocopherol, also play a crucial role in maintaining ROS levels by acting as redox buffers in plant cells. In contrast to ROS, the mechanisms of NO synthesis in plant cells are not yet fully understood, constituting one of the major challenges to studies investigating this signaling molecule. Apparently, the action of nitrate reductase NR , a cytosolic enzyme essential for the assimilation of nitrogen, also represents an important source of NO for plants Horchani et al.

It has been suggested that NR is involved in the production of NO during a variety of physiological processes, such as bacterial defense Modolo et al. However, under normal growth conditions, NR preferentially reduces nitrate to nitrite, and NR is only able to generate significant amounts of NO under certain conditions, such as anaerobic conditions or high concentrations of nitrite Gupta et al. There have been numerous reports of an arginine-dependent nitric oxide synthase NOS in extracts of different plant species Jasid et al.

In addition to biosynthetic processes, another crucial factor in NO concentration in the cell is the formation of S -nitrosothiols, particularly S -nitrosoglutathione GSNO , relatively stable molecules in solution that may act as reservoirs of NO Leterrier et al. GSNO also regulates the NO concentration in the cell via inhibition of the nitrogen assimilation pathways Fungillo et al.

Degradation of NO is as important as synthesis and transport in determining the final concentration of this signal molecule in plant cells. Recently, Sanz-Luque et al.

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Another class of hemoglobins, the non-symbiotic hemoglobins nsHb , particularly those belonging to the GLB1 class, have also been reported to have NO dioxygenase activity and to promote the degradation of NO in certain circumstances, such as hypoxia Perazzolli et al. The reduction in GLB1 expression, moreover, allows NO concentration to increase, triggering defense responses against stress Mur et al. ROS are well-known inducers of NO synthesis in various plant species exposed to abiotic stress, although the signaling involved in this process is still not completely understood.

In fact, the activation of antioxidant mechanisms to maintain ROS homeostasis often involves the participation of NO Farnese et al. Some studies, however, have suggested that NO can inhibit the antioxidant capacity of the cell Marti et al. These seemingly contradictory results may be due to the dose-dependent effects of NO on cellular redox status. According to this hypothesis, low concentrations of NO stimulate the antioxidant system and promote adaptation to stress conditions, while high concentrations of NO trigger severe cell damage and even cell death Thomas et al.

The mode of action of ROS and NO at the molecular level was and still is the subject of many studies, both in plants and other organisms, such as mammals and bacteria Green et al. The available data indicate that the effects of NO, as well as certain species derived from this molecule, depend on chemical changes in proteins, which can occur by three different mechanisms: metal nitrosylation, tyrosine nitration, and S -nitrosylation Lamotte et al.

Metal nitrosylation consists of NO binding to transition metals in metalloproteins. Soluble guanylate cyclase is an example of an enzyme that is modulated by this type of post-translational modification. Tyrosine nitration is the addition of a nitro group to tyrosine residues.

Although tyrosine nitration was originally considered indicative of stress, recent evidence suggests its involvement in cell signaling Mengel et al. Finally, S -nitrosylation, which consists of NO binding to cysteine residues in target proteins, is apparently the principal mechanism for the transduction of the NO bioactivity. S -nitrosylation can also occur via trans -nitrosylation, that is, by the transfer of NO from an S -nitrosylated residue to another thiol group through the action of low-molecular weight nitrosothiols, such as GSNO Lamotte et al.

Regardless of the mechanism involved, S -nitrosylation is a post-translational modification that can alter the activity, stability, conformation, interactions with other molecules or subcellular localization of the target protein, regulating a wide range of cellular functions and signaling events Sevilla et al.

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S -nitrosylation is an important process in plant responses to abiotic stress. Exposure to salt stress, for example, results in the S -nitrosylation of enzymes involved in different physiological processes, such as respiration, photorespiration, and antioxidant pathways Camejo et al. S -nitrosylation of proteins that participate in central processes in the plant cell presumably contributes to the metabolic reprogramming required to maintain homeostasis under stress conditions. In addition to changes in cellular enzyme dynamics, S -nitrosylation may also trigger changes in gene expression as a result of S -nitrosylation of transcription factors, affecting their affinity for DNA or their location.

Recently, it was demonstrated that S -nitrosylation is a negative regulator of transcription factors from the MYB family regulator of tolerance to biotic and abiotic stresses , which may be important for the inactivation of this regulatory protein after the initial response of plants to stress Tavares et al.

Several S -nitrosylated nuclear proteins have also been identified, including histone deacetylases, which highlights the regulatory role of NO in events located in the nucleus Chaki et al. Histone deacetylases are responsible for the removal of acetyl groups on histones, promoting the chromatin condensation, which makes the genes less accessible to the transcriptional machinery Mengel et al. In mammalian cells, S -nitrosylated histone deacetylases become detached from the chromatin, increasing acetylation and gene expression Nott et al. Thus, the S -nitrosylation of deacetylases suggests that NO participates in the regulation of epigenetic processes in plants Floryszak-Wieczorek et al.

The S -nitrosylation state of any protein is determined by the balance between nitrosylation and denitrosylation reactions. In fact, denitrosylation, which involves the removal of NO from cysteine residues, is essential for the reversibility of S -nitrosylation and influences the enzyme activity, protein—protein interactions and many other aspects of signaling Sevilla et al. Although this process has been more extensively studied in mammals, recent evidence has shown that it occurs in plant cells Kneeshaw et al.

Thus, the control of the redox status of thiol groups depends on their interaction with NO and with the denitrosylation systems, which influences the intensity and duration of the signaling events Benhar, As observed for NO, ROS also transmit signals via post-translational modifications in proteins and, once more, cysteine residues are the main targets.

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However, while NO promotes S -nitrosylation, ROS can trigger a diverse range of oxidative post-translational modifications Ox-PTM , reversible or irreversible, including S -glutathionylation, disulfide bond formation, and sulfhydration Akter et al. This modification is highly unstable and will lead to subsequent changes; the major ones are the reaction with free protein thiols to form disulfide bonds or the covalent attachment of low-molecular weight thiols, such as GSH, promoting S -glutathionylation, a process that is important in signaling and protein protection against superoxide.

The reduction of disulfide bonds and deglutathionylation interrupt the signal that initiated with the Ox-PTMs and are controlled by glutaredoxins and thioredoxin, respectively Waszczak et al. The Ox-PTMs, particularly S -glutathionylation, play a central role in the response to abiotic stresses and can modulate numerous cellular processes affecting proteins, transcription factors, and chromatin structure. These mechanisms, however, have mostly been studied in animals and bacteria, and many aspects of the Ox-PTM-mediated responses are unknown in plants Zagorchev et al. Its translocation to the nucleus activates the expression of hypoxia-responsive genes.

In the presence of oxygen, however, ERFVII cysteine residues are oxidized to sulfenic acid, conjugated with arginine and directed to degradation, down-regulating the expression of genes that are no longer needed Dietz, The Ox-PTMs can also be positive regulators of gene transcription, as in the case of transcription factors of heat shock proteins HSF , whose oxidation by H 2 O 2 induces translocation from the cytosol to the nucleus Habibi, Despite the growing number of studies, however, there is still little information about the effects of S -nitrosylation and Ox-PTMs on gene expression and the consequences of these changes on plant metabolism in stress conditions.

Thus, the molecular mechanisms involved in cell signaling mediated by ROS and NO are still far from being fully understood. Traditionally, heavy metals are considered those chemicals that have a density higher than 5 g cm -3 or an atomic number higher than In plant physiology, however, the term heavy metal has been used generically to refer to any metal or metalloid that is toxic to plants, even when present at low concentrations Singh et al.


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Although some of the members of this group are necessary for growth and development, others have no known function in plant cells and, regardless of their physiological role, the accumulation of metals usually results in severe cell damage, which can lead to the death of the plant Besson-Bard et al.

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