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      Targeted for destruction: degradation of singlet oxygen-damaged chloroplasts

      research-article
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      Plant Signaling & Behavior
      Taylor & Francis
      Autophagy, cellular degradation, chloroplast, photosynthesis, reactive oxygen species, signaling

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          ABSTRACT

          Photosynthesis is an essential process that plants must regulate to survive in dynamic environments. Thus, chloroplasts (the sites of photosynthesis in plant and algae cells) use multiple signaling mechanisms to report their health to the cell. Such signals are poorly understood but often involve reactive oxygen species (ROS) produced from the photosynthetic light reactions. One ROS, singlet oxygen ( 1O 2), can signal to initiate chloroplast degradation, but the cellular machinery involved in identifying and degrading damaged chloroplasts ( i.e., chloroplast quality control pathways) is unknown. To provide mechanistic insight into these pathways, two recent studies have investigated degrading chloroplasts in the Arabidopsis thaliana 1O 2 over-producing plastid ferrochelatase two ( fc2) mutant. First, a structural analysis of degrading chloroplasts was performed with electron microscopy, which demonstrated that damaged chloroplasts can protrude into the central vacuole compartment with structures reminiscent of fission-type microautophagy. 1O 2-stressed chloroplasts swelled before these interactions, which may be a mechanism for their selective degradation. Second, the roles of autophagosomes and canonical autophagy (macroautophagy) were shown to be dispensable for 1O 2-initiated chloroplast degradation. Instead, putative fission-type microautophagy genes were induced by chloroplast 1O 2. Here, we discuss how these studies implicate this poorly understood cellular degradation pathway in the dismantling of 1O 2-damaged chloroplasts.

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          Most cited references25

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          Mitophagy and Quality Control Mechanisms in Mitochondrial Maintenance.

          The maintenance of a healthy and functional mitochondrial network is critical during development as well as throughout life in the response to physiological adaptations and stress conditions. Owing to their role in energy production, mitochondria are exposed to high levels of reactive oxygen species, making them particularly vulnerable to mitochondrial DNA mutations and protein misfolding. Given that mitochondria are formed from proteins encoded by both nuclear and mitochondrial genomes, an additional layer of complexity is inherent in the coordination of protein synthesis and the mitochondrial import of nuclear-encoded proteins. For these reasons, mitochondria have evolved multiple systems of quality control to ensure that the requisite number of functional mitochondria are present to meet the demands of the cell. These pathways work to eliminate damaged mitochondrial proteins or parts of the mitochondrial network by mitophagy and renew components by adding protein and lipids through biogenesis, collectively resulting in mitochondrial turnover. Mitochondrial quality control mechanisms are multi-tiered, operating at the protein, organelle and cell levels. Herein, we discuss mitophagy in different physiological contexts and then relate it to other quality control pathways, including the unfolded protein response, shedding of vesicles, proteolysis, and degradation by the ubiquitin-proteasome system. Understanding how these pathways contribute to the maintenance of mitochondrial homeostasis could provide insights into the development of targeted treatments when these systems fail in disease.
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            Production and scavenging of reactive oxygen species in chloroplasts and their functions.

            Kozi Asada (2006)
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              Singlet oxygen: there is indeed something new under the sun.

              Singlet oxygen, O(2)(a(1)Delta(g)), the lowest excited electronic state of molecular oxygen, has been known to the scientific community for approximately 80 years. It has a characteristic chemistry that sets it apart from the triplet ground state of molecular oxygen, O(2)(X(3)Sigma), and is important in fields that range from atmospheric chemistry and materials science to biology and medicine. For such a "mature citizen", singlet oxygen nevertheless remains at the cutting-edge of modern science. In this critical review, recent work on singlet oxygen is summarized, focusing primarily on systems that involve light. It is clear that there is indeed still something new under the sun (243 references).
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                Author and article information

                Journal
                Plant Signal Behav
                Plant Signal Behav
                Plant Signaling & Behavior
                Taylor & Francis
                1559-2316
                1559-2324
                8 June 2022
                2022
                8 June 2022
                : 17
                : 1
                : 2084955
                Affiliations
                [0001]The School of Plant Sciences, University of Arizona; , Tucson, AZ, USA
                Author notes
                CONTACT Jesse D. Woodson jessewoodson@ 123456email.arizona.edu The School of Plant Sciences, University of Arizona; , 303 Forbes Hall, 1140 E. South Campus Drive, Tucson, AZ 85721-0036, USA
                Author information
                https://orcid.org/0000-0002-9680-0656
                https://orcid.org/0000-0002-5463-5146
                Article
                2084955
                10.1080/15592324.2022.2084955
                9196835
                35676885
                acce22cd-b2d1-490e-aab0-6873e834f63b
                © 2022 The Author(s). Published with license by Taylor & Francis Group, LLC.

                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 use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 2, References: 25, Pages: 1
                Categories
                Research Article
                Short Communication

                Plant science & Botany
                autophagy,cellular degradation,chloroplast,photosynthesis,reactive oxygen species,signaling

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