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      Post-translational coordination of chlorophyll biosynthesis and breakdown by BCMs maintains chlorophyll homeostasis during leaf development

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          Abstract

          Chlorophyll is indispensable for life on Earth. Dynamic control of chlorophyll level, determined by the relative rates of chlorophyll anabolism and catabolism, ensures optimal photosynthesis and plant fitness. How plants post-translationally coordinate these two antagonistic pathways during their lifespan remains enigmatic. Here, we show that two Arabidopsis paralogs of BALANCE of CHLOROPHYLL METABOLISM (BCM) act as functionally conserved scaffold proteins to regulate the trade-off between chlorophyll synthesis and breakdown. During early leaf development, BCM1 interacts with GENOMES UNCOUPLED 4 to stimulate Mg-chelatase activity, thus optimizing chlorophyll synthesis. Meanwhile, BCM1’s interaction with Mg-dechelatase promotes degradation of the latter, thereby preventing chlorophyll degradation. At the onset of leaf senescence, BCM2 is up-regulated relative to BCM1, and plays a conserved role in attenuating chlorophyll degradation. These results support a model in which post-translational regulators promote chlorophyll homeostasis by adjusting the balance between chlorophyll biosynthesis and breakdown during leaf development.

          Abstract

          Plants regulate chlorophyll levels to optimise photosynthesis. Here Wang et al. describe two paralogous thylakoid proteins, BCM1 and BCM2, which stimulate chlorophyll biosynthesis and attenuate chlorophyll degradation respectively through interaction with the Mg-chelatase-stimulating factor GUN4 and Mg-dechelatase isoform SGR1.

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          Reactive oxygen species: metabolism, oxidative stress, and signal transduction.

          Several reactive oxygen species (ROS) are continuously produced in plants as byproducts of aerobic metabolism. Depending on the nature of the ROS species, some are highly toxic and rapidly detoxified by various cellular enzymatic and nonenzymatic mechanisms. Whereas plants are surfeited with mechanisms to combat increased ROS levels during abiotic stress conditions, in other circumstances plants appear to purposefully generate ROS as signaling molecules to control various processes including pathogen defense, programmed cell death, and stomatal behavior. This review describes the mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions. New insights into the complexity and roles that ROS play in plants have come from genetic analyses of ROS detoxifying and signaling mutants. Considering recent ROS-induced genome-wide expression analyses, the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.
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            Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis.

            The transient gene expression system using Arabidopsis mesophyll protoplasts has proven an important and versatile tool for conducting cell-based experiments using molecular, cellular, biochemical, genetic, genomic and proteomic approaches to analyze the functions of diverse signaling pathways and cellular machineries. A well-established protocol that has been extensively tested and applied in numerous experiments is presented here. The method includes protoplast isolation, PEG-calcium transfection of plasmid DNA and protoplast culture. Physiological responses and high-throughput capability enable facile and cost-effective explorations as well as hypothesis-driven tests. The protoplast isolation and DNA transfection procedures take 6-8 h, and the results can be obtained in 2-24 h. The cell system offers reliable guidelines for further comprehensive analysis of complex regulatory mechanisms in whole-plant physiology, immunity, growth and development.
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              Leaf senescence.

              Leaf senescence constitutes the final stage of leaf development and is critical for plants' fitness as nutrient relocation from leaves to reproducing seeds is achieved through this process. Leaf senescence involves a coordinated action at the cellular, tissue, organ, and organism levels under the control of a highly regulated genetic program. Major breakthroughs in the molecular understanding of leaf senescence were achieved through characterization of various senescence mutants and senescence-associated genes, which revealed the nature of regulatory factors and a highly complex molecular regulatory network underlying leaf senescence. The genetically identified regulatory factors include transcription regulators, receptors and signaling components for hormones and stress responses, and regulators of metabolism. Key issues still need to be elucidated, including cellular-level analysis of senescence-associated cell death, the mechanism of coordination among cellular-, organ-, and organism-level senescence, the integration mechanism of various senescence-affecting signals, and the nature and control of leaf age.
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                Author and article information

                Contributors
                wangp2014@gmail.com
                bernhard.grimm@rz.hu-berlin.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                20 March 2020
                20 March 2020
                2020
                : 11
                : 1254
                Affiliations
                [1 ]ISNI 0000 0001 2248 7639, GRID grid.7468.d, Institute of Biology/Plant Physiology, , Humboldt-Universität zu Berlin, ; Philippstraße 13, 10115 Berlin, Germany
                [2 ]ISNI 0000 0004 0467 6972, GRID grid.7384.8, Zellbiologie/Elektronenmikroskopie, , Universität Bayreuth, ; 95440 Bayreuth, Germany
                [3 ]ISNI 0000 0001 2248 7639, GRID grid.7468.d, Present Address: Institute of Biology/Physiology of Plant Cell Organelles, , Humboldt-Universität zu Berlin, ; Philippstraße 13, 10115 Berlin, Germany
                Author information
                http://orcid.org/0000-0001-8420-5326
                http://orcid.org/0000-0002-2293-7297
                http://orcid.org/0000-0002-4166-8563
                Article
                14992
                10.1038/s41467-020-14992-9
                7083845
                32198392
                e2973eae-9766-49fc-95a6-146217e535c6
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 30 July 2019
                : 11 February 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: WA 4599/2-1
                Award ID: FOR2092, GE 1110/9-1
                Award ID: SFB TRR175, subproject C04
                Award ID: FOR2092, GR 936/18-1
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100005156, Alexander von Humboldt-Stiftung (Alexander von Humboldt Foundation);
                Funded by: FundRef https://doi.org/10.13039/501100008848, State Ministry of Education and Culture, Science and the Arts | Elitenetzwerk Bayern (Elite Network of Bavaria);
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                plant sciences,photosynthesis,plant physiology
                Uncategorized
                plant sciences, photosynthesis, plant physiology

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