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      Key players of singlet oxygen-induced cell death in plants

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          Abstract

          The production of reactive oxygen species (ROS) is an unavoidable consequence of oxygenic photosynthesis. Singlet oxygen ( 1O 2) is a highly reactive species to which has been attributed a major destructive role during the execution of ROS-induced cell death in photosynthetic tissues exposed to excess light. The study of the specific biological activity of 1O 2 in plants has been hindered by its high reactivity and short lifetime, the concurrent production of other ROS under photooxidative stress, and limited in vivo detection methods. However, during the last 15 years, the isolation and characterization of two 1O 2-overproducing mutants in Arabidopsis thaliana, flu and ch1, has allowed the identification of genetically controlled 1O 2 cell death pathways and a 1O 2 acclimation pathway that are triggered at sub-cytotoxic concentrations of 1O 2. The study of flu has revealed the control of cell death by the plastid proteins EXECUTER (EX)1 and EX2. In ch1, oxidized derivatives of β-carotene, such as β-cyclocitral and dihydroactinidiolide, have been identified as important upstream messengers in the 1O 2 signaling pathway that leads to stress acclimation. In both the flu and ch1 mutants, phytohormones act as important promoters or inhibitors of cell death. In particular, jasmonate has emerged as a key player in the decision between acclimation and cell death in response to 1O 2. Although the flu and ch1 mutants show many similarities, especially regarding their gene expression profiles, key differences, such as EXECUTER-independent cell death in ch1, have also been observed and will need further investigation to be fully understood.

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          H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.

          Microbial elicitors or attempted infection with an avirulent pathogen strain causes the rapid production of reactive oxygen intermediates. We report here that H2O2 from this oxidative burst not only drives the cross-linking of cell wall structural proteins, but also functions as a local trigger of programmed death in challenged cells and as a diffusible signal for the induction in adjacent cells of genes encoding cellular protectants such as glutathione S-transferase and glutathione peroxidase. Thus, H2O2 from the oxidative burst plays a key role in the orchestration of a localized hypersensitive response during the expression of plant disease resistance.
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            Essential versus accessory aspects of cell death: recommendations of the NCCD 2015

            Cells exposed to extreme physicochemical or mechanical stimuli die in an uncontrollable manner, as a result of their immediate structural breakdown. Such an unavoidable variant of cellular demise is generally referred to as ‘accidental cell death' (ACD). In most settings, however, cell death is initiated by a genetically encoded apparatus, correlating with the fact that its course can be altered by pharmacologic or genetic interventions. ‘Regulated cell death' (RCD) can occur as part of physiologic programs or can be activated once adaptive responses to perturbations of the extracellular or intracellular microenvironment fail. The biochemical phenomena that accompany RCD may be harnessed to classify it into a few subtypes, which often (but not always) exhibit stereotyped morphologic features. Nonetheless, efficiently inhibiting the processes that are commonly thought to cause RCD, such as the activation of executioner caspases in the course of apoptosis, does not exert true cytoprotective effects in the mammalian system, but simply alters the kinetics of cellular demise as it shifts its morphologic and biochemical correlates. Conversely, bona fide cytoprotection can be achieved by inhibiting the transduction of lethal signals in the early phases of the process, when adaptive responses are still operational. Thus, the mechanisms that truly execute RCD may be less understood, less inhibitable and perhaps more homogeneous than previously thought. Here, the Nomenclature Committee on Cell Death formulates a set of recommendations to help scientists and researchers to discriminate between essential and accessory aspects of cell death.
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              Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants.

              (1)O(2) (singlet oxygen) is a reactive O(2) species produced from triplet excited chlorophylls in the chloroplasts, especially when plants are exposed to excess light energy. Similarly to other active O(2) species, (1)O(2) has a dual effect: It is toxic, causing oxidation of biomolecules, and it can act as a signal molecule that leads to cell death or to acclimation. Carotenoids are considered to be the main (1)O(2) quenchers in chloroplasts, and we show here that light stress induces the oxidation of the carotenoid β-carotene in Arabidopsis plants, leading to the accumulation of different volatile derivatives. One such compound, β-cyclocitral, was found to induce changes in the expression of a large set of genes that have been identified as (1)O(2) responsive genes. In contrast, β-cyclocitral had little effect on the expression of H(2)O(2) gene markers. β-Cyclocitral-induced reprogramming of gene expression was associated with an increased tolerance to photooxidative stress. The results indicate that β-cyclocitral is a stress signal produced in high light that is able to induce defense mechanisms and represents a likely messenger involved in the (1)O(2) signaling pathway in plants.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                04 February 2015
                2015
                : 6
                : 39
                Affiliations
                [1] 1Laboratoire de Génétique et Biophysique des Plantes, Institut de Biologie Environnementale et Biotechnologie, Commissariat à l’Énergie Atomique et aux Énergies Alternatives Marseille, France
                [2] 2CNRS, UMR 7265 Biologie Végétale et Microbiologie Environnementales Marseille, France
                [3] 3Aix Marseille Université Marseille, France
                [4] 4Laboratoire d’Ecophysiologie Moléculaire des Plantes, Institut de Biologie Environnementale et Biotechnologie, Commissariat à l’Énergie Atomique et aux Énergies Alternatives Saint-Paul-lez-Durance, France
                Author notes

                Edited by: Antoine Danon, Institut de Biologie Physico-Chimique, France

                Reviewed by: Bartolome Sabater, Universidad de Alcala, Spain; Robert Fluhr, Weizmann Institute of Science, Israel; Anja Liszkay, Centre National de la Recherche Scientifique, France

                *Correspondence: Christophe Laloi, Laboratoire de Génétique et Biophysique des Plantes, Institut de Biologie Environnementale et Biotechnologie, Commissariat à l’Énergie Atomique et aux nergies Alternatives, F -13009 Marseille, France e-mail: christophe.laloi@ 123456univ-amu.fr ; Michel Havaux, Laboratoire d’Ecophysiologie Moléculaire des Plantes, Institut de Biologie Environnementale et Biotechnologie, Commissariat à l’Énergie Atomique et aux Énergies Alternatives, F-13108 Saint-Paul-lez-Durance, France e-mail: michel.havaux@ 123456cea.fr

                This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science.

                Article
                10.3389/fpls.2015.00039
                4316694
                25699067
                d2424eb1-9903-4162-80d6-b596c4953fdb
                Copyright © 2015 Laloi and Havaux.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 December 2014
                : 15 January 2015
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 72, Pages: 9, Words: 0
                Categories
                Plant Science
                Review Article

                Plant science & Botany
                singlet oxygen,oxidative stress,cell death,acclimation,executer,β-cyclocitral,phytohormones,oxylipins

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