Nitric Oxide (NO) and Hydrogen Sulfide (H2S) in Higher Plants under Physiological and Stress Conditions

A special issue of Antioxidants (ISSN 2076-3921). This special issue belongs to the section "ROS, RNS and RSS".

Deadline for manuscript submissions: closed (15 May 2019) | Viewed by 45629

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Dear Colleagues,

Nitric oxide (NO) and hydrogen sulfide (H2S) are two gasotransmitters endogenously generated in plant cells. These molecules share diverse plant functions and participate in a wide range of physiological processes including seed germination, root architecture, plant growth and development, stomatal movement, and senescence or fruit ripening among others, as well as in the mechanism of response against environmental stresses. Both gasotransmitters have families of related molecules designated reactive nitrogen species (RNS) and reactive sulfur species (RSS). Their mechanism of action is through posttranslational modifications such as S-nitrosation, nitration, or persulfidation affecting the redox status and function of the target proteins. Thus, NO and H2S mediate several signaling networks and are key elements in biochemistry and physiology of plants.

The present Special Issue of Antioxidants aims to provide the most recent findings about the function of these two gasotransmitters in higher plants and it is opened to different types of manuscripts including original research papers, perspectives, or reviews where either NO, H2S, or related molecules could be involved at biochemical or physiological levels.

Prof. Dr. Francisco J. Corpas
Guest Editor

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Published Papers (8 papers)

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Editorial

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3 pages, 331 KiB  
Editorial
Nitric Oxide and Hydrogen Sulfide in Higher Plants under Physiological and Stress Conditions
by Francisco J. Corpas
Antioxidants 2019, 8(10), 457; https://doi.org/10.3390/antiox8100457 - 7 Oct 2019
Cited by 27 | Viewed by 2919
Abstract
Nitric oxide (NO) and hydrogen sulfide (H2S) are two gasotransmitters endogenously generated in plant cells [...] Full article
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Research

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11 pages, 2802 KiB  
Article
d-Cysteine-Induced Rapid Root Abscission in the Water Fern Azolla Pinnata: Implications for the Linkage between d-Amino Acid and Reactive Sulfur Species (RSS) in Plant Environmental Responses
by Hideo Yamasaki, Masahiro P. Ogura, Katsumi A. Kingjoe and Michael F. Cohen
Antioxidants 2019, 8(9), 411; https://doi.org/10.3390/antiox8090411 - 18 Sep 2019
Cited by 38 | Viewed by 4919
Abstract
Reactive Oxygen Species (ROS) and Reactive Nitrogen Species (RNS) have been proposed as universal signaling molecules in plant stress responses. There are a growing number of studies suggesting that hydrogen sulfide (H2S) or Reactive Sulfur Species (RSS) are also involved in [...] Read more.
Reactive Oxygen Species (ROS) and Reactive Nitrogen Species (RNS) have been proposed as universal signaling molecules in plant stress responses. There are a growing number of studies suggesting that hydrogen sulfide (H2S) or Reactive Sulfur Species (RSS) are also involved in plant abiotic as well as biotic stress responses. However, it is still a matter of debate as to how plants utilize those RSS in their signaling cascades. Here, we demonstrate that d-cysteine is a novel candidate for bridging our gap in understanding. In the genus of the tiny water-floating fern Azolla, a rapid root abscission occurs in response to a wide variety of environmental stimuli as well as chemical inducers. We tested five H2S chemical donors, Na2S, GYY4137, 5a, 8l, and 8o, and found that 5a showed a significant abscission activity. Root abscission also occurred with the polysulfides Na2S2, Na2S3, and Na2S4. Rapid root abscission comparable to other known chemical inducers was observed in the presence of d-cysteine, whereas l-cysteine showed no effect. We suggest that d-cysteine is a physiologically relevant substrate to induce root abscission in the water fern Azolla. Full article
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16 pages, 5179 KiB  
Article
Regulation of Hydrogen Sulfide Metabolism by Nitric Oxide Inhibitors and the Quality of Peaches during Cold Storage
by Biao Geng, Dandan Huang and Shuhua Zhu
Antioxidants 2019, 8(9), 401; https://doi.org/10.3390/antiox8090401 - 16 Sep 2019
Cited by 36 | Viewed by 4164
Abstract
Both nitric oxide (NO) and hydrogen sulfide (H2S) have been shown to have positive effects on the maintenance of fruit quality during storage; however, the mechanisms by which NO regulates the endogenous H2S metabolism remain unknown. In this experiment, [...] Read more.
Both nitric oxide (NO) and hydrogen sulfide (H2S) have been shown to have positive effects on the maintenance of fruit quality during storage; however, the mechanisms by which NO regulates the endogenous H2S metabolism remain unknown. In this experiment, peaches were immersed in solutions of NO, potassium 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (c-PTIO, as an NO scavenger), N-nitro-l-arginine methyl ester (l-NAME, as an inhibitor of nitric oxide synthase (NOS)-like activity), and sodium tungstate (as an inhibitor of nitrate reductase), and the resulting changes in the H2S metabolism of peaches were studied. The results showed that exogenous NO reduced the contents of endogenous H2S, Cys, and sulfite; decreased the activities of l-/d-cysteine desulfhydrase (l-/d-CD), O-acetylserine (thiol)lyase (OAS-TL), and sulfite reductase (SiR); and increased the activity of β-cyanoalanine synthase (β-CAS). Both c-PTIO and sodium tungstate had similar roles in increasing the H2S content by sustaining the activities of l-/d-CDs, OAS-TL, and SiR. l-NAME increased the H2S content, mainly by maintaining the d-CD activity. The results suggest that NO, c-PTIO, l-NAME, and sodium tungstate differently regulate the H2S metabolism of peaches during storage. Full article
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18 pages, 3973 KiB  
Article
Sweet Pepper (Capsicum annuum L.) Fruits Contain an Atypical Peroxisomal Catalase That Is Modulated by Reactive Oxygen and Nitrogen Species
by Marta Rodríguez-Ruiz, Salvador González-Gordo, Amanda Cañas, María Jesús Campos, Alberto Paradela, Francisco J. Corpas and José M. Palma
Antioxidants 2019, 8(9), 374; https://doi.org/10.3390/antiox8090374 - 4 Sep 2019
Cited by 48 | Viewed by 10157
Abstract
During the ripening of sweet pepper (Capsicum annuum L.) fruits, in a genetically controlled scenario, enormous metabolic changes occur that affect the physiology of most cell compartments. Peroxisomal catalase gene expression decreases after pepper fruit ripening, while the enzyme is also susceptible [...] Read more.
During the ripening of sweet pepper (Capsicum annuum L.) fruits, in a genetically controlled scenario, enormous metabolic changes occur that affect the physiology of most cell compartments. Peroxisomal catalase gene expression decreases after pepper fruit ripening, while the enzyme is also susceptible to undergo post-translational modifications (nitration, S-nitrosation, and oxidation) promoted by reactive oxygen and nitrogen species (ROS/RNS). Unlike most plant catalases, the pepper fruit enzyme acts as a homodimer, with an atypical native molecular mass of 125 to 135 kDa and an isoelectric point of 7.4, which is higher than that of most plant catalases. These data suggest that ROS/RNS could be essential to modulate the role of catalase in maintaining basic cellular peroxisomal functions during pepper fruit ripening when nitro-oxidative stress occurs. Using catalase from bovine liver as a model and biotin-switch labeling, in-gel trypsin digestion, and nanoliquid chromatography coupled with mass spectrometry, it was found that Cys377 from the bovine enzyme could potentially undergo S-nitrosation. To our knowledge, this is the first report of a cysteine residue from catalase that can be post-translationally modified by S-nitrosation, which makes it especially important to find the target points where the enzyme can be modulated under either physiological or adverse conditions. Full article
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16 pages, 2390 KiB  
Article
Polyamine Induction in Postharvest Banana Fruits in Response to NO Donor SNP Occurs via l-Arginine Mediated Pathway and Not via Competitive Diversion of S-Adenosyl-l-Methionine
by Veeresh Lokesh, Girigowda Manjunatha, Namratha S. Hegde, Mallesham Bulle, Bijesh Puthusseri, Kapuganti Jagadis Gupta and Bhagyalakshmi Neelwarne
Antioxidants 2019, 8(9), 358; https://doi.org/10.3390/antiox8090358 - 1 Sep 2019
Cited by 16 | Viewed by 4715
Abstract
Nitric oxide (NO) is known to antagonize ethylene by various mechanisms; one of such mechanisms is reducing ethylene levels by competitive action on S-adenosyl-L-methionine (SAM)—a common precursor for both ethylene and polyamines (PAs) biosynthesis. In order to investigate whether this mechanism of SAM [...] Read more.
Nitric oxide (NO) is known to antagonize ethylene by various mechanisms; one of such mechanisms is reducing ethylene levels by competitive action on S-adenosyl-L-methionine (SAM)—a common precursor for both ethylene and polyamines (PAs) biosynthesis. In order to investigate whether this mechanism of SAM pool diversion by NO occur towards PAs biosynthesis in banana, we studied the effect of NO on alterations in the levels of PAs, which in turn modulate ethylene levels during ripening. In response to NO donor sodium nitroprusside (SNP) treatment, all three major PAs viz. putrescine, spermidine and spermine were induced in control as well as ethylene pre-treated banana fruits. However, the gene expression studies in two popular banana varieties of diverse genomes, Nanjanagudu rasabale (NR; AAB genome) and Cavendish (CAV; AAA genome) revealed the downregulation of SAM decarboxylase, an intermediate gene involved in ethylene and PA pathway after the fifth day of NO donor SNP treatment, suggesting that ethylene and PA pathways do not compete for SAM. Interestingly, arginine decarboxylase belonging to arginine-mediated route of PA biosynthesis was upregulated several folds in response to the SNP treatment. These observations revealed that NO induces PAs via l-arginine-mediated route and not via diversion of SAM pool. Full article
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12 pages, 3207 KiB  
Article
Ectopic or Over-Expression of Class 1 Phytoglobin Genes Confers Flooding Tolerance to the Root Nodules of Lotus japonicus by Scavenging Nitric Oxide
by Mitsutaka Fukudome, Eri Watanabe, Ken-ichi Osuki, Nahoko Uchi and Toshiki Uchiumi
Antioxidants 2019, 8(7), 206; https://doi.org/10.3390/antiox8070206 - 4 Jul 2019
Cited by 14 | Viewed by 4464
Abstract
Flooding limits biomass production in agriculture. Leguminous plants, important agricultural crops, use atmospheric dinitrogen gas as nitrogen nutrition by symbiotic nitrogen fixation with rhizobia, but this root-nodule symbiosis is sometimes broken down by flooding of the root system. In this study, we analyzed [...] Read more.
Flooding limits biomass production in agriculture. Leguminous plants, important agricultural crops, use atmospheric dinitrogen gas as nitrogen nutrition by symbiotic nitrogen fixation with rhizobia, but this root-nodule symbiosis is sometimes broken down by flooding of the root system. In this study, we analyzed the effect of flooding on the symbiotic system of transgenic Lotus japonicus lines which overexpressed class 1 phytoglobin (Glb1) of L. japonicus (LjGlb1-1) or ectopically expressed that of Alnus firma (AfGlb1). In the roots of wild-type plants, flooding increased nitric oxide (NO) level and expression of senescence-related genes and decreased nitrogenase activity; in the roots of transgenic lines, these effects were absent or less pronounced. The decrease of chlorophyll content in leaves and the increase of reactive oxygen species (ROS) in roots and leaves caused by flooding were also suppressed in these lines. These results suggest that increased levels of Glb1 help maintain nodule symbiosis under flooding by scavenging NO and controlling ROS. Full article
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11 pages, 1707 KiB  
Article
NADPH Oxidase (Rboh) Activity is Up Regulated during Sweet Pepper (Capsicum annuum L.) Fruit Ripening
by Ángela Chu-Puga, Salvador González-Gordo, Marta Rodríguez-Ruiz, José M. Palma and Francisco J. Corpas
Antioxidants 2019, 8(1), 9; https://doi.org/10.3390/antiox8010009 - 1 Jan 2019
Cited by 57 | Viewed by 6961
Abstract
In plants, NADPH oxidase (NOX) is also known as a respiratory burst oxidase homolog (Rboh). This highly important enzyme, one of the main enzymatic sources of superoxide radicals (O2), is involved in the metabolism of reactive oxygen and nitrogen [...] Read more.
In plants, NADPH oxidase (NOX) is also known as a respiratory burst oxidase homolog (Rboh). This highly important enzyme, one of the main enzymatic sources of superoxide radicals (O2), is involved in the metabolism of reactive oxygen and nitrogen species (ROS and RNS), which is active in the non-climacteric pepper (Capsicum annuum L.) fruit. We used sweet pepper fruits at two ripening stages (green and red) to biochemically analyze the O2-generating Rboh activity and the number of isozymes during this physiological process. Malondialdehyde (MDA) content, an oxidative stress marker, was also assayed as an index of lipid peroxidation. In red fruits, MDA was observed to increase 2-fold accompanied by a 5.3-fold increase in total Rboh activity. Using in-gel assays of Rboh activity, we identified a total of seven CaRboh isozymes (I–VII) which were differentially modulated during ripening. CaRboh-III and CaRboh-I were the most prominent isozymes in green and red fruits, respectively. An in vitro assay showed that CaRboh activity is inhibited in the presence of nitric oxide (NO) donors, peroxynitrite (ONOO) and glutathione (GSH), suggesting that CaRboh can undergo S-nitrosation, Tyr-nitration, and glutathionylation, respectively. In summary, this study provides a basic biochemical characterization of CaRboh activity in pepper fruits and indicates that this O2-generating Rboh is involved in nitro-oxidative stress associated with sweet pepper fruit ripening. Full article
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Review

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22 pages, 1385 KiB  
Review
Gasotransmitters in Action: Nitric Oxide-Ethylene Crosstalk during Plant Growth and Abiotic Stress Responses
by Zsuzsanna Kolbert, Gábor Feigl, Luciano Freschi and Péter Poór
Antioxidants 2019, 8(6), 167; https://doi.org/10.3390/antiox8060167 - 8 Jun 2019
Cited by 48 | Viewed by 6381
Abstract
Since their first description as atmospheric gases, it turned out that both nitric oxide (NO) and ethylene (ET) are multifunctional plant signals. ET and polyamines (PAs) use the same precursor for their synthesis, and NO can be produced from PA oxidation. Therefore, an [...] Read more.
Since their first description as atmospheric gases, it turned out that both nitric oxide (NO) and ethylene (ET) are multifunctional plant signals. ET and polyamines (PAs) use the same precursor for their synthesis, and NO can be produced from PA oxidation. Therefore, an indirect metabolic link between NO and ET synthesis can be considered. NO signal is perceived primarily through S-nitrosation without the involvement of a specific receptor, while ET signal is sensed by a well-characterized receptor complex. Both NO and ET are synthetized by plants at various developmental stages (e.g., seeds, fruits) and as a response to numerous environmental factors (e.g., heat, heavy metals) and they mutually regulate each other’s levels. Most of the growth and developmental processes (e.g., fruit ripening, de-etiolation) are regulated by NO–ET antagonism, while in abiotic stress responses, both antagonistic (e.g., dark-induced stomatal opening, cadmium-induced cell death) and synergistic (e.g., UV-B-induced stomatal closure, iron deficiency-induced expression of iron acquisition genes) NO–ET interplays have been revealed. Despite the numerous pieces of experimental evidence revealing NO–ET relationships in plants, the picture is far from complete. Understanding the mechanisms of NO–ET interactions may contribute to the increment of yield and intensification of stress tolerance of crop plants in changing environments. Full article
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