Nitric Oxide Signaling in Plants

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Physiology and Metabolism".

Deadline for manuscript submissions: closed (31 March 2019) | Viewed by 60495

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Guest Editor
School of Applied Sciences, University of the West of England, Bristol, UK
Interests: redox signaling; reactive oxygen species; hydrogen sulfide; hydrogen gas; nitric oxide
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Guest Editor
Faculty of Health and Applied Sciences, University of the West of England, Bristol, UK
Interests: abscisic acid (ABA) signaling; stomatal mechanisms; nitric oxide; reactive oxygen species; drought stress

Special Issue Information

Dear Colleagues,

Nitric oxide (NO) is a gaseous reactive molecule which is a key component of plant cell signaling mechanisms. NO is involved in the breaking of seed germination, the growth and development of the plant as well as flower senescence and formation of root nodules in legumes. Stress responses of plants, such as drought and pathogen challenge, involve the generation and accumulation of NO in plant cells. NO can be produced in plant cells by several mechanisms, one of the main sources being the enzyme nitrate reductase. Being relatively reactive NO can interact with superoxide anions to produce peroxynitrite, or with hydrogen sulfide to create nitrosothiols, both which can control cellular events. NO once produced can react with a variety of downstream protein targets. These include proteins which contain iron, often within heme, such as guanylyl cyclase and leghemoglobin which may lead to further signaling or NO removal. Modification of thiol groups of proteins by NO, a process known as S-nitrosation (or S-nitrosylation) is a key mechanism by which signaling is propagated in cells. This protein modification can be reversed by SNO-reductases, allowing such signaling to be toggled on and off. This Special Issue of Plants will highlight the production and roles of NO in plants, along with the ways NO can interact with other reactive signaling molecules, leading to coordinated signaling events in plants.

Prof. John Hancock
Guest Editor

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Keywords

  • nitric oxide
  • reactive oxygen species
  • stress responses
  • S-nitrosation
  • S-nitrosylation
  • thiol modification
  • nitrate reductase
  • SNO-reductase

Published Papers (10 papers)

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Editorial

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5 pages, 207 KiB  
Editorial
Nitric Oxide Signaling in Plants
by John T. Hancock
Plants 2020, 9(11), 1550; https://doi.org/10.3390/plants9111550 - 12 Nov 2020
Cited by 17 | Viewed by 2223
Abstract
Nitric oxide (NO) is an integral part of cell signaling mechanisms in animals and plants. In plants, its enzymatic generation is still controversial. Evidence points to nitrate reductase being important, but the presence of a nitric oxide synthase-like enzyme is still contested. Regardless, [...] Read more.
Nitric oxide (NO) is an integral part of cell signaling mechanisms in animals and plants. In plants, its enzymatic generation is still controversial. Evidence points to nitrate reductase being important, but the presence of a nitric oxide synthase-like enzyme is still contested. Regardless, NO has been shown to mediate many developmental stages in plants, and to be involved in a range of physiological responses, from stress management to stomatal aperture closure. Downstream from its generation are alterations of the actions of many cell signaling components, with post-translational modifications of proteins often being key. Here, a collection of papers embraces the differing aspects of NO metabolism in plants. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)

Research

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22 pages, 2786 KiB  
Article
Nitric Oxide Overproduction by cue1 Mutants Differs on Developmental Stages and Growth Conditions
by Tamara Lechón, Luis Sanz, Inmaculada Sánchez-Vicente and Oscar Lorenzo
Plants 2020, 9(11), 1484; https://doi.org/10.3390/plants9111484 - 4 Nov 2020
Cited by 7 | Viewed by 3222
Abstract
The cue1 nitric oxide (NO) overproducer mutants are impaired in a plastid phosphoenolpyruvate/phosphate translocator, mainly expressed in Arabidopsis thaliana roots. cue1 mutants present an increased content of arginine, a precursor of NO in oxidative synthesis processes. However, the pathways of plant NO biosynthesis [...] Read more.
The cue1 nitric oxide (NO) overproducer mutants are impaired in a plastid phosphoenolpyruvate/phosphate translocator, mainly expressed in Arabidopsis thaliana roots. cue1 mutants present an increased content of arginine, a precursor of NO in oxidative synthesis processes. However, the pathways of plant NO biosynthesis and signaling have not yet been fully characterized, and the role of CUE1 in these processes is not clear. Here, in an attempt to advance our knowledge regarding NO homeostasis, we performed a deep characterization of the NO production of four different cue1 alleles (cue1-1, cue1-5, cue1-6 and nox1) during seed germination, primary root elongation, and salt stress resistance. Furthermore, we analyzed the production of NO in different carbon sources to improve our understanding of the interplay between carbon metabolism and NO homeostasis. After in vivo NO imaging and spectrofluorometric quantification of the endogenous NO levels of cue1 mutants, we demonstrate that CUE1 does not directly contribute to the rapid NO synthesis during seed imbibition. Although cue1 mutants do not overproduce NO during germination and early plant development, they are able to accumulate NO after the seedling is completely established. Thus, CUE1 regulates NO homeostasis during post-germinative growth to modulate root development in response to carbon metabolism, as different sugars modify root elongation and meristem organization in cue1 mutants. Therefore, cue1 mutants are a useful tool to study the physiological effects of NO in post-germinative growth. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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15 pages, 1794 KiB  
Article
Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation
by Joana R. Expósito, Sara Martín San Román, Eva Barreno, José Reig-Armiñana, Francisco José García-Breijo and Myriam Catalá
Plants 2019, 8(7), 189; https://doi.org/10.3390/plants8070189 - 26 Jun 2019
Cited by 10 | Viewed by 4308
Abstract
Lichens are poikilohydrous symbiotic associations between a fungus, photosynthetic partners, and bacteria. They are tolerant to repeated desiccation/rehydration cycles and adapted to anhydrobiosis. Nitric oxide (NO) is a keystone for stress tolerance of lichens; during lichen rehydration, NO limits free radicals and lipid [...] Read more.
Lichens are poikilohydrous symbiotic associations between a fungus, photosynthetic partners, and bacteria. They are tolerant to repeated desiccation/rehydration cycles and adapted to anhydrobiosis. Nitric oxide (NO) is a keystone for stress tolerance of lichens; during lichen rehydration, NO limits free radicals and lipid peroxidation but no data on the mechanisms of its synthesis exist. The aim of this work is to characterize the synthesis of NO in the lichen Ramalina farinacea using inhibitors of nitrate reductase (NR) and nitric oxide synthase (NOS), tungstate, and NG-nitro-L-arginine methyl ester (L-NAME), respectively. Tungstate suppressed the NO level in the lichen and caused an increase in malondialdehyde during rehydration in the hyphae of cortex and in phycobionts, suggesting that a plant-like NR is involved in the NO production. Specific activity of NR in R. farinacea was 91 μU/mg protein, a level comparable to those in the bryophyte Physcomitrella patens and Arabidopsis thaliana. L-NAME treatment did not suppress the NO level in the lichens. On the other hand, NADPH-diaphorase activity cytochemistry showed a possible presence of a NOS-like activity in the microalgae where it is associated with cytoplasmatic vesicles. These data provide initial evidence that NO synthesis in R. farinacea involves NR. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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15 pages, 2319 KiB  
Article
Isoform-Specific NO Synthesis by Arabidopsis thaliana Nitrate Reductase
by Marie Agatha Mohn, Besarta Thaqi and Katrin Fischer-Schrader
Plants 2019, 8(3), 67; https://doi.org/10.3390/plants8030067 - 16 Mar 2019
Cited by 51 | Viewed by 5986
Abstract
Nitrate reductase (NR) is important for higher land plants, as it catalyzes the rate-limiting step in the nitrate assimilation pathway, the two-electron reduction of nitrate to nitrite. Furthermore, it is considered to be a major enzymatic source of the important signaling molecule nitric [...] Read more.
Nitrate reductase (NR) is important for higher land plants, as it catalyzes the rate-limiting step in the nitrate assimilation pathway, the two-electron reduction of nitrate to nitrite. Furthermore, it is considered to be a major enzymatic source of the important signaling molecule nitric oxide (NO), that is produced in a one-electron reduction of nitrite. Like many other plants, the model plant Arabidopsis thaliana expresses two isoforms of NR (NIA1 and NIA2). Up to now, only NIA2 has been the focus of detailed biochemical studies, while NIA1 awaits biochemical characterization. In this study, we have expressed and purified functional fragments of NIA1 and subjected them to various biochemical assays for comparison with the corresponding NIA2-fragments. We analyzed the kinetic parameters in multiple steady-state assays using nitrate or nitrite as substrate and measured either substrate consumption (nitrate or nitrite) or product formation (NO). Our results show that NIA1 is the more efficient nitrite reductase while NIA2 exhibits higher nitrate reductase activity, which supports the hypothesis that the isoforms have special functions in the plant. Furthermore, we successfully restored the physiological electron transfer pathway of NR using reduced nicotinamide adenine dinucleotide (NADH) and nitrate or nitrite as substrates by mixing the N-and C-terminal fragments of NR, thus, opening up new possibilities to study NR activity, regulation and structure. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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Review

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17 pages, 3049 KiB  
Review
Nitrogen Dioxide at Ambient Concentrations Induces Nitration and Degradation of PYR/PYL/RCAR Receptors to Stimulate Plant Growth: A Hypothetical Model
by Misa Takahashi and Hiromichi Morikawa
Plants 2019, 8(7), 198; https://doi.org/10.3390/plants8070198 - 30 Jun 2019
Cited by 9 | Viewed by 3947
Abstract
Exposing Arabidopsis thaliana (Arabidopsis) seedlings fed with soil nitrogen to 10–50 ppb nitrogen dioxide (NO2) for several weeks stimulated the uptake of major elements, photosynthesis, and cellular metabolisms to more than double the biomass of shoot, total leaf area and contents [...] Read more.
Exposing Arabidopsis thaliana (Arabidopsis) seedlings fed with soil nitrogen to 10–50 ppb nitrogen dioxide (NO2) for several weeks stimulated the uptake of major elements, photosynthesis, and cellular metabolisms to more than double the biomass of shoot, total leaf area and contents of N, C P, K, S, Ca and Mg per shoot relative to non-exposed control seedlings. The 15N/14N ratio analysis by mass spectrometry revealed that N derived from NO2 (NO2-N) comprised < 5% of the total plant N, showing that the contribution of NO2-N as N source was minor. Moreover, histological analysis showed that leaf size and biomass were increased upon NO2 treatment, and that these increases were attributable to leaf age-dependent enhancement of cell proliferation and enlargement. Thus, NO2 may act as a plant growth signal rather than an N source. Exposure of Arabidopsis leaves to 40 ppm NO2 induced virtually exclusive nitration of PsbO and PsbP proteins (a high concentration of NO2 was used). The PMF analysis identified the ninth tyrosine residue of PsbO1 (9Tyr) as a nitration site. 9Tyr of PsbO1 was exclusively nitrated after incubation of the thylakoid membranes with a buffer containing NO2 and NO2 or a buffer containing NO2 alone. Nitration was catalyzed by illumination and repressed by photosystem II (PSII) electron transport inhibitors, and decreased oxygen evolution. Thus, protein tyrosine nitration altered (downregulated) the physiological function of cellular proteins of Arabidopsis leaves. This indicates that NO2-induced protein tyrosine nitration may stimulate plant growth. We hypothesized that atmospheric NO2 at ambient concentrations may induce tyrosine nitration of PYR/PYL/RCAR receptors in Arabidopsis leaves, followed by degradation of PYR/PYL/RCAR, upregulation of target of rapamycin (TOR) regulatory complexes, and stimulation of plant growth. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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21 pages, 3799 KiB  
Review
Post-Translational Modification of Proteins Mediated by Nitro-Fatty Acids in Plants: Nitroalkylation
by Lorena Aranda-Caño, Beatriz Sánchez-Calvo, Juan C. Begara-Morales, Mounira Chaki, Capilla Mata-Pérez, María N. Padilla, Raquel Valderrama and Juan B. Barroso
Plants 2019, 8(4), 82; https://doi.org/10.3390/plants8040082 - 29 Mar 2019
Cited by 24 | Viewed by 5905
Abstract
Nitrate fatty acids (NO2-FAs) are considered reactive lipid species derived from the non-enzymatic oxidation of polyunsaturated fatty acids by nitric oxide (NO) and related species. Nitrate fatty acids are powerful biological electrophiles which can react with biological nucleophiles such as glutathione [...] Read more.
Nitrate fatty acids (NO2-FAs) are considered reactive lipid species derived from the non-enzymatic oxidation of polyunsaturated fatty acids by nitric oxide (NO) and related species. Nitrate fatty acids are powerful biological electrophiles which can react with biological nucleophiles such as glutathione and certain protein–amino acid residues. The adduction of NO2-FAs to protein targets generates a reversible post-translational modification called nitroalkylation. In different animal and human systems, NO2-FAs, such as nitro-oleic acid (NO2-OA) and conjugated nitro-linoleic acid (NO2-cLA), have cytoprotective and anti-inflammatory influences in a broad spectrum of pathologies by modulating various intracellular pathways. However, little knowledge on these molecules in the plant kingdom exists. The presence of NO2-OA and NO2-cLA in olives and extra-virgin olive oil and nitro-linolenic acid (NO2-Ln) in Arabidopsis thaliana has recently been detected. Specifically, NO2-Ln acts as a signaling molecule during seed and plant progression and beneath abiotic stress events. It can also release NO and modulate the expression of genes associated with antioxidant responses. Nevertheless, the repercussions of nitroalkylation on plant proteins are still poorly known. In this review, we demonstrate the existence of endogenous nitroalkylation and its effect on the in vitro activity of the antioxidant protein ascorbate peroxidase. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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13 pages, 672 KiB  
Review
Role of Nitrate Reductase in NO Production in Photosynthetic Eukaryotes
by Manuel Tejada-Jimenez, Angel Llamas, Aurora Galván and Emilio Fernández
Plants 2019, 8(3), 56; https://doi.org/10.3390/plants8030056 - 6 Mar 2019
Cited by 52 | Viewed by 12284
Abstract
Nitric oxide is a gaseous secondary messenger that is critical for proper cell signaling and plant survival when exposed to stress. Nitric oxide (NO) synthesis in plants, under standard phototrophic oxygenic conditions, has long been a very controversial issue. A few algal strains [...] Read more.
Nitric oxide is a gaseous secondary messenger that is critical for proper cell signaling and plant survival when exposed to stress. Nitric oxide (NO) synthesis in plants, under standard phototrophic oxygenic conditions, has long been a very controversial issue. A few algal strains contain NO synthase (NOS), which appears to be absent in all other algae and land plants. The experimental data have led to the hypothesis that molybdoenzyme nitrate reductase (NR) is the main enzyme responsible for NO production in most plants. Recently, NR was found to be a necessary partner in a dual system that also includes another molybdoenzyme, which was renamed NO-forming nitrite reductase (NOFNiR). This enzyme produces NO independently of the molybdenum center of NR and depends on the NR electron transport chain from NAD(P)H to heme. Under the circumstances in which NR is not present or active, the existence of another NO-forming system that is similar to the NOS system would account for NO production and NO effects. PII protein, which senses and integrates the signals of the C–N balance in the cell, likely has an important role in organizing cell responses. Here, we critically analyze these topics. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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19 pages, 1147 KiB  
Review
S-Nitrosoglutathione Reductase—The Master Regulator of Protein S-Nitrosation in Plant NO Signaling
by Jana Jahnová, Lenka Luhová and Marek Petřivalský
Plants 2019, 8(2), 48; https://doi.org/10.3390/plants8020048 - 21 Feb 2019
Cited by 84 | Viewed by 6694
Abstract
S-nitrosation has been recognized as an important mechanism of protein posttranslational regulations, based on the attachment of a nitroso group to cysteine thiols. Reversible S-nitrosation, similarly to other redox-base modifications of protein thiols, has a profound effect on protein structure and activity and [...] Read more.
S-nitrosation has been recognized as an important mechanism of protein posttranslational regulations, based on the attachment of a nitroso group to cysteine thiols. Reversible S-nitrosation, similarly to other redox-base modifications of protein thiols, has a profound effect on protein structure and activity and is considered as a convergence of signaling pathways of reactive nitrogen and oxygen species. In plant, S-nitrosation is involved in a wide array of cellular processes during normal development and stress responses. This review summarizes current knowledge on S-nitrosoglutathione reductase (GSNOR), a key enzyme which regulates intracellular levels of S-nitrosoglutathione (GSNO) and indirectly also of protein S-nitrosothiols. GSNOR functions are mediated by its enzymatic activity, which catalyzes irreversible GSNO conversion to oxidized glutathione within the cellular catabolism of nitric oxide. GSNOR is involved in the maintenance of balanced levels of reactive nitrogen species and in the control of cellular redox state. Multiple functions of GSNOR in plant development via NO-dependent and -independent signaling mechanisms and in plant defense responses to abiotic and biotic stress conditions have been uncovered. Extensive studies of plants with down- and upregulated GSNOR, together with application of transcriptomics and proteomics approaches, seem promising for new insights into plant S-nitrosothiol metabolism and its regulation. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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14 pages, 2450 KiB  
Review
Nitric Oxide: Its Generation and Interactions with Other Reactive Signaling Compounds
by John T. Hancock and Steven J. Neill
Plants 2019, 8(2), 41; https://doi.org/10.3390/plants8020041 - 12 Feb 2019
Cited by 78 | Viewed by 6075
Abstract
Nitric oxide (NO) is an immensely important signaling molecule in animals and plants. It is involved in plant reproduction, development, key physiological responses such as stomatal closure, and cell death. One of the controversies of NO metabolism in plants is the identification of [...] Read more.
Nitric oxide (NO) is an immensely important signaling molecule in animals and plants. It is involved in plant reproduction, development, key physiological responses such as stomatal closure, and cell death. One of the controversies of NO metabolism in plants is the identification of enzymatic sources. Although there is little doubt that nitrate reductase (NR) is involved, the identification of a nitric oxide synthase (NOS)-like enzyme remains elusive, and it is becoming increasingly clear that such a protein does not exist in higher plants, even though homologues have been found in algae. Downstream from its production, NO can have several potential actions, but none of these will be in isolation from other reactive signaling molecules which have similar chemistry to NO. Therefore, NO metabolism will take place in an environment containing reactive oxygen species (ROS), hydrogen sulfide (H2S), glutathione, other antioxidants and within a reducing redox state. Direct reactions with NO are likely to produce new signaling molecules such as peroxynitrite and nitrosothiols, and it is probable that chemical competitions will exist which will determine the ultimate end result of signaling responses. How NO is generated in plants cells and how NO fits into this complex cellular environment needs to be understood. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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10 pages, 654 KiB  
Review
Impact of Nitric Oxide (NO) on the ROS Metabolism of Peroxisomes
by Francisco J. Corpas, Luis A. del Río and José M. Palma
Plants 2019, 8(2), 37; https://doi.org/10.3390/plants8020037 - 10 Feb 2019
Cited by 43 | Viewed by 7180
Abstract
Nitric oxide (NO) is a gaseous free radical endogenously generated in plant cells. Peroxisomes are cell organelles characterized by an active metabolism of reactive oxygen species (ROS) and are also one of the main cellular sites of NO production in higher plants. In [...] Read more.
Nitric oxide (NO) is a gaseous free radical endogenously generated in plant cells. Peroxisomes are cell organelles characterized by an active metabolism of reactive oxygen species (ROS) and are also one of the main cellular sites of NO production in higher plants. In this mini-review, an updated and comprehensive overview is presented of the evidence available demonstrating that plant peroxisomes have the capacity to generate NO, and how this molecule and its derived products, peroxynitrite (ONOO) and S-nitrosoglutathione (GSNO), can modulate the ROS metabolism of peroxisomes, mainly throughout protein posttranslational modifications (PTMs), including S-nitrosation and tyrosine nitration. Several peroxisomal antioxidant enzymes, such as catalase (CAT), copper-zinc superoxide dismutase (CuZnSOD), and monodehydroascorbate reductase (MDAR), have been demonstrated to be targets of NO-mediated PTMs. Accordingly, plant peroxisomes can be considered as a good example of the interconnection existing between ROS and reactive nitrogen species (RNS), where NO exerts a regulatory function of ROS metabolism acting upstream of H2O2. Full article
(This article belongs to the Special Issue Nitric Oxide Signaling in Plants)
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