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Nitric oxide signaling, metabolism and toxicity in nitrogen-fixing symbiosis.
Berger, A, Boscari, A, Frendo, P, Brouquisse, R
Journal of experimental botany. 2019;(17):4505-4520
Abstract
Interactions between legumes and rhizobia lead to the establishment of a symbiotic relationship characterized by the formation of a new organ, the nodule, which facilitates the fixation of atmospheric nitrogen (N2) by nitrogenase through the creation of a hypoxic environment. Significant amounts of nitric oxide (NO) accumulate at different stages of nodule development, suggesting that NO performs specific signaling and/or metabolic functions during symbiosis. NO, which regulates nodule gene expression, accumulates to high levels in hypoxic nodules. NO accumulation is considered to assist energy metabolism within the hypoxic environment of the nodule via a phytoglobin-NO-mediated respiration process. NO is a potent inhibitor of the activity of nitrogenase and other plant and bacterial enzymes, acting as a developmental signal in the induction of nodule senescence. Hence, key questions concern the relative importance of the signaling and metabolic functions of NO versus its toxic action and how NO levels are regulated to be compatible with nitrogen fixation functions. This review analyses these paradoxical roles of NO at various stages of symbiosis, and highlights the role of plant phytoglobins and bacterial hemoproteins in the control of NO accumulation.
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Plant peroxisomes at the crossroad of NO and H2 O2 metabolism.
Corpas, FJ, Del Río, LA, Palma, JM
Journal of integrative plant biology. 2019;(7):803-816
Abstract
Plant peroxisomes are subcellular compartments involved in many biochemical pathways during the life cycle of a plant but also in the mechanism of response against adverse environmental conditions. These organelles have an active nitro-oxidative metabolism under physiological conditions but this could be exacerbated under stress situations. Furthermore, peroxisomes have the capacity to proliferate and also undergo biochemical adaptations depending on the surrounding cellular status. An important characteristic of peroxisomes is that they have a dynamic metabolism of reactive nitrogen and oxygen species (RNS and ROS) which generates two key molecules, nitric oxide (NO) and hydrogen peroxide (H2 O2 ). These molecules can exert signaling functions by means of post-translational modifications that affect the functionality of target molecules like proteins, peptides or fatty acids. This review provides an overview of the endogenous metabolism of ROS and RNS in peroxisomes with special emphasis on polyamine and uric acid metabolism as well as the possibility that these organelles could be a source of signal molecules involved in the functional interconnection with other subcellular compartments.
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Sulfur: the heart of nitric oxide-dependent redox signalling.
Umbreen, S, Lubega, J, Loake, GJ
Journal of experimental botany. 2019;(16):4279-4286
Abstract
Nitric oxide (NO), more benign than its more reactive and damaging related molecules, reactive oxygen species (ROS), is perfectly suited for duties as a redox signalling molecule. A key route for NO bioactivity is through S-nitrosation, the addition of an NO moiety to a protein Cys thiol (-SH). This redox-based, post-translational modification (PTM) can modify protein function analogous to more well established PTMs such as phosphorylation, for example by modulating enzyme activity, localization, or protein-protein interactions. At the heart of the underpinning chemistry associated with this PTM is sulfur. The emerging evidence suggests that S-nitrosation is integral to a myriad of plant biological processes embedded in both development and environmental relations. However, a role for S-nitrosation is perhaps most well established in plant-pathogen interactions.
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Advances in research on treatment of heart failure with nitrosyl hydrogen.
Guo, Y, Xu, J, Wu, L, Deng, Y, Wang, J, An, J
Heart failure reviews. 2019;(6):941-948
Abstract
Heart failure is the end stage of various heart diseases such as ischemic heart disease, dilated cardiomyopathy, valvular heart disease, congenital heart disease, and hypertensive myocardial damage. It is characterized by a decrease in myocardial contractility, but there is currently no ideal treatment. Nitroxyl hydrogen (HNO) is considered to be a protonated form of NO. It has special chemical properties compared to other nitrogen oxides. In the body of organisms, HNO can participate in all aspects of the occurrence and development of heart failure (HF) and react with some proteins closely related to cardiac activity, changing its spatial structure and exerting cardioprotective effects. In recent years, studies have shown that HNO can inhibit cardiomyocyte hypertrophy, reduce inflammation, enhance myocardial contractility, dilate coronary arteries as well as peripheral blood vessels in early heart failure, and protect the heart against heart failure. This paper, combined with the latest research results at home and abroad, clarifies that nitrosyl hydrogen exerts cardioprotective effects through various processes that occur in the development of heart failure.
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5.
Tolerance of roots to low oxygen: 'Anoxic' cores, the phytoglobin-nitric oxide cycle, and energy or oxygen sensing.
Armstrong, W, Beckett, PM, Colmer, TD, Setter, TL, Greenway, H
Journal of plant physiology. 2019;:92-108
Abstract
Acclimation by plants to hypoxia and anoxia is of importance in various ecological systems, and especially for roots in waterlogged soil. We present evidence for acclimation by roots via 'anoxic' cores rather than being triggered by O2 sensors. The evidence for 'anoxic' cores comes from radial O2 profiles across maize roots and associated metabolic changes such as increases in the 'anaerobic enzymes' ADH and PDC in the 'anoxic' core, and inhibition of Cl- transport to the xylem. These cores are predicted to develop within 15-20 min after sudden transfer of a root to hypoxia, so that the cores are 'anoxically-shocked'. We suggest that 'anoxic' cores could emanate a signal(s), such as ACC the precursor of ethylene and/or propagation of a 'Ca2+ wave', to other tissue zones. There, the signalling would result in acclimation of the tissues to energy crisis metabolism. An O2 diffusion model for tissues with an 'anoxic' core, indicates that the phytoglobin-nitric oxide (Pgb-NO) cycle would only be engaged in a thin 'shell' (annulus) of tissue surrounding the 'anoxic' core, and so would only contribute small amounts of ATP on a whole organ basis (e.g. whole roots). A key feature within this annulus of tissue, where O2 is likely to be limiting, is that the ratio (ATP formed) / (O2 consumed) is 5-6, both when the NAD(P)H of glycolysis is converted to NAD(P)+ by the Pgb-NO cycle or by the TCA cycle linked to the electron transport chain. The main function of the Pgb-NO cycle may be the modulating of NO levels and O2 scavenging, thus preventing oxidative damage. We speculate that an 'anoxic' core in hypoxic plant organs may have a particularly high tolerance to anoxia because cells might receive a prolonged supply of carbohydrates and/or ATP from the regions still receiving sufficient O2 for oxidative phosphorylation. Severely hypoxic or 'anoxic' cores are well documented, but much research on responses of roots to hypoxia is still based on bulk tissue analyses. More research is needed on the interaction between 'anoxic' cores and tissues still receiving sufficient O2 for oxidative phosphorylation, both during a hypoxic exposure and during subsequent anoxia of the tissue/organ as a whole.
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6.
Nitric oxide is a suppressor of aluminum-induced mitochondria and caspase-like protease-dependent programmed cell death in plants.
He, H, He, LF
Plant signaling & behavior. 2019;(9):1640566
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Abstract
Aluminum (Al) promotes programmed cell death (PCD) in plants. Although a lot of knowledge about the mechanisms of Al tolerance has been learned, how Al-induced PCD is regulated by nitric oxide (NO) is poorly understood. Mitochondrion is the regulatory center for PCD. We found that Al reduced the level of mitochondrial NO/H2O2, promoted the opening of mitochondrial permeability transition pore, decreased mitochondrial inner membrane potential (∆ψm), and increased caspase-like protease activity. NO-specific scavenger cPTIO enhanced these effects that were reversed by NO donor sodium nitroprusside. Our data suggest that NO suppresses Al-induced PCD by improving mitochondrial physiological properties.
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Considerations of the importance of redox state for reactive nitrogen species action.
Hancock, JT
Journal of experimental botany. 2019;(17):4323-4331
Abstract
Nitric oxide (NO) and other reactive nitrogen species (RNS) are immensely important signalling molecules in plants, being involved in a range of physiological responses. However, the exact way in which NO fits into signal transduction pathways is not always easy to understand. Here, some of the issues that should be considered are discussed. This includes how NO may interact directly with other reactive signals, such as reactive oxygen and sulfur species, how NO metabolism is almost certainly compartmentalized, that threshold levels of RNS may need to be reached to have effects, and how the intracellular redox environment may impact on NO signalling. Until better tools are available to understand how NO is generated in cells, where it accumulates, and to what levels it reaches, it will be hard to get a full understanding of NO signalling. The interaction of RNS metabolism with the intracellular redox environment needs further investigation. A changing redox poise will impact on whether RNS species can thrive in or around cells. Such mechanisms will determine whether specific RNS can indeed control the responses needed by a cell.
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Strigolactone-nitric oxide interplay in plants: The story has just begun.
Kolbert, Z
Physiologia plantarum. 2019;(3):487-497
Abstract
Both strigolactones (SLs) and nitric oxide (NO) are regulatory signals with diverse roles during plant development and stress responses. This review aims to discuss the so far available data regarding SLs-NO interplay in plant systems. The majority of the few articles dealing with SL-NO interplay focuses on the root system and it seems that NO can be an upstream negative regulator of SL biosynthesis or an upstream positive regulator of SL signaling depending on the nutrient supply. From the so far published results it is clear that NO modifies the activity of target proteins involved in SL biosynthesis or signaling which may be a physiologically relevant interaction. Therefore, in silico analysis of NO-dependent posttranslational modifications in SL-related proteins was performed using computational prediction tools and putative NO-target proteins were specified. The picture is presumably more complicated, since also SL is able to modify NO levels. As a confirmation, author detected NO levels in different organs of max1-1 and max2-1 Arabidopsis and compared to the wild-type these mutants showed enhanced NO levels in their root tips indicating the negative effect of endogenous SLs on NO metabolism. Exogenous SL analogue-triggered NO production seems to contradict the results of the genetic study, which is an inconsistency should be taken into consideration in the future. In the coming years, the link between SL and NO signaling in further physiological processes should be examined and the possibilities of NO-dependent posttranslational modifications of SL biosynthetic and signaling proteins should be looked more closely.
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Nitric oxide and plant mineral nutrition: current knowledge.
Buet, A, Galatro, A, Ramos-Artuso, F, Simontacchi, M
Journal of experimental botany. 2019;(17):4461-4476
Abstract
Plants under conditions of essential mineral deficiency trigger signaling mechanisms that involve common components. Among these components, nitric oxide (NO) has been identified as a key participant in responses to changes in nutrient availability. Usually, nutrient imbalances affect the levels of NO in specific plant tissues, via modification of its rate of synthesis or degradation. Changes in the level of NO affect plant morphology and/or trigger responses associated with nutrient homeostasis, mediated by its interaction with reactive oxygen species, phytohormones, and through post-translational modification of proteins. NO-related events constitute an exciting field of research to understand how plants adapt and respond to conditions of nutrient shortage. This review summarizes the current knowledge on NO as a component of the multiple processes related to plant performance under conditions of deficiency in mineral nutrients, focusing on macronutrients such as nitrogen, phosphate, potassium, and magnesium, as well as micronutrients such as iron and zinc.
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10.
Nitric oxide molecular targets: reprogramming plant development upon stress.
Sánchez-Vicente, I, Fernández-Espinosa, MG, Lorenzo, O
Journal of experimental botany. 2019;(17):4441-4460
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Abstract
Plants are sessile organisms that need to complete their life cycle by the integration of different abiotic and biotic environmental signals, tailoring developmental cues and defense concomitantly. Commonly, stress responses are detrimental to plant growth and, despite the fact that intensive efforts have been made to understand both plant development and defense separately, most of the molecular basis of this trade-off remains elusive. To cope with such a diverse range of processes, plants have developed several strategies including the precise balance of key plant growth and stress regulators [i.e. phytohormones, reactive nitrogen species (RNS), and reactive oxygen species (ROS)]. Among RNS, nitric oxide (NO) is a ubiquitous gasotransmitter involved in redox homeostasis that regulates specific checkpoints to control the switch between development and stress, mainly by post-translational protein modifications comprising S-nitrosation of cysteine residues and metals, and nitration of tyrosine residues. In this review, we have sought to compile those known NO molecular targets able to balance the crossroads between plant development and stress, with special emphasis on the metabolism, perception, and signaling of the phytohormones abscisic acid and salicylic acid during abiotic and biotic stress responses.