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      The hypoxia–reoxygenation stress in plants

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          Abstract

          Plants are very plastic in adapting growth and development to changing adverse environmental conditions. This feature will be essential for plants to survive climate changes characterized by extreme temperatures and rainfall. Although plants require molecular oxygen (O 2) to live, they can overcome transient low-O 2 conditions (hypoxia) until return to standard 21% O 2 atmospheric conditions (normoxia). After heavy rainfall, submerged plants in flooded lands undergo transient hypoxia until water recedes and normoxia is recovered. The accumulated information on the physiological and molecular events occurring during the hypoxia phase contrasts with the limited knowledge on the reoxygenation process after hypoxia, which has often been overlooked in many studies in plants. Phenotypic alterations during recovery are due to potentiated oxidative stress generated by simultaneous reoxygenation and reillumination leading to cell damage. Besides processes such as N-degron proteolytic pathway-mediated O 2 sensing, or mitochondria-driven metabolic alterations, other molecular events controlling gene expression have been recently proposed as key regulators of hypoxia and reoxygenation. RNA regulatory functions, chromatin remodeling, protein synthesis, and post-translational modifications must all be studied in depth in the coming years to improve our knowledge on hypoxia–reoxygenation transition in plants, a topic with relevance in agricultural biotechnology in the context of global climate change.

          Abstract

          Plant responses to hypoxia and subsequent reoxygenation occur through a network of processes involving oxygen sensing, RNA function, chromatin remodeling, gene expression, and protein synthesis, which together allow plants to either escape or tolerate the stress.

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          Most cited references187

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          Reperfusion injury and reactive oxygen species: The evolution of a concept☆

          Reperfusion injury, the paradoxical tissue response that is manifested by blood flow-deprived and oxygen-starved organs following the restoration of blood flow and tissue oxygenation, has been a focus of basic and clinical research for over 4-decades. While a variety of molecular mechanisms have been proposed to explain this phenomenon, excess production of reactive oxygen species (ROS) continues to receive much attention as a critical factor in the genesis of reperfusion injury. As a consequence, considerable effort has been devoted to identifying the dominant cellular and enzymatic sources of excess ROS production following ischemia-reperfusion (I/R). Of the potential ROS sources described to date, xanthine oxidase, NADPH oxidase (Nox), mitochondria, and uncoupled nitric oxide synthase have gained a status as the most likely contributors to reperfusion-induced oxidative stress and represent priority targets for therapeutic intervention against reperfusion-induced organ dysfunction and tissue damage. Although all four enzymatic sources are present in most tissues and are likely to play some role in reperfusion injury, priority and emphasis has been given to specific ROS sources that are enriched in certain tissues, such as xanthine oxidase in the gastrointestinal tract and mitochondria in the metabolically active heart and brain. The possibility that multiple ROS sources contribute to reperfusion injury in most tissues is supported by evidence demonstrating that redox-signaling enables ROS produced by one enzymatic source (e.g., Nox) to activate and enhance ROS production by a second source (e.g., mitochondria). This review provides a synopsis of the evidence implicating ROS in reperfusion injury, the clinical implications of this phenomenon, and summarizes current understanding of the four most frequently invoked enzymatic sources of ROS production in post-ischemic tissue.
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            Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization.

            The majority of eukaryotic organisms rely on molecular oxygen for respiratory energy production. When the supply of oxygen is compromised, a variety of acclimation responses are activated to reduce the detrimental effects of energy depletion. Various oxygen-sensing mechanisms have been described that are thought to trigger these responses, but they each seem to be kingdom specific and no sensing mechanism has been identified in plants until now. Here we show that one branch of the ubiquitin-dependent N-end rule pathway for protein degradation, which is active in both mammals and plants, functions as an oxygen-sensing mechanism in Arabidopsis thaliana. We identified a conserved amino-terminal amino acid sequence of the ethylene response factor (ERF)-transcription factor RAP2.12 to be dedicated to an oxygen-dependent sequence of post-translational modifications, which ultimately lead to degradation of RAP2.12 under aerobic conditions. When the oxygen concentration is low-as during flooding-RAP2.12 is released from the plasma membrane and accumulates in the nucleus to activate gene expression for hypoxia acclimation. Our discovery of an oxygen-sensing mechanism opens up new possibilities for improving flooding tolerance in crops. © 2011 Macmillan Publishers Limited. All rights reserved
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              Ecophysiology. Climate change tightens a metabolic constraint on marine habitats.

              Warming of the oceans and consequent loss of dissolved oxygen (O2) will alter marine ecosystems, but a mechanistic framework to predict the impact of multiple stressors on viable habitat is lacking. Here, we integrate physiological, climatic, and biogeographic data to calibrate and then map a key metabolic index-the ratio of O2 supply to resting metabolic O2 demand-across geographic ranges of several marine ectotherms. These species differ in thermal and hypoxic tolerances, but their contemporary distributions are all bounded at the equatorward edge by a minimum metabolic index of ~2 to 5, indicative of a critical energetic requirement for organismal activity. The combined effects of warming and O2 loss this century are projected to reduce the upper ocean's metabolic index by ~20% globally and by ~50% in northern high-latitude regions, forcing poleward and vertical contraction of metabolically viable habitats and species ranges.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                J Exp Bot
                J Exp Bot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                11 August 2021
                24 December 2020
                24 December 2020
                : 72
                : 16 , Special Issue: Plant Responses to Environmental Stress
                : 5841-5856
                Affiliations
                [1 ]Instituto de Biología Molecular y Celular de Plantas (Consejo Superior de Investigaciones Científicas – Universidad Politécnica de Valencia) , Valencia, Spain
                [2 ]University of Birmingham , UK
                Author notes
                Author information
                https://orcid.org/0000-0002-7332-1572
                https://orcid.org/0000-0002-9647-0896
                https://orcid.org/0000-0003-4073-6867
                Article
                eraa591
                10.1093/jxb/eraa591
                8355755
                33367851
                11f1ba82-5c8b-4e05-92dd-8569dc16cc5a
                © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 October 2020
                : 10 December 2020
                : 16 December 2020
                : 04 February 2021
                Page count
                Pages: 16
                Funding
                Funded by: Ministerio de Ciencia e Innovación, DOI 10.13039/501100004837;
                Award ID: BIO2017-82945-P
                Categories
                Review Papers
                AcademicSubjects/SCI01210

                Plant science & Botany
                development,flooding,hypoxia,mitochondria,nitric oxide,oxidative stress,oxygen sensing,phytohormones,reillumination,reoxygenation,submergence,waterlogging

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