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      Chlorophyll Breakdown in Senescent Banana Leaves: Catabolism Reprogrammed for Biosynthesis of Persistent Blue Fluorescent Tetrapyrroles

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          Abstract

          Chlorophyll breakdown is a visual phenomenon of leaf senescence and fruit ripening. It leads to the formation of colorless chlorophyll catabolites, a group of (chlorophyll-derived bilin-type) linear tetrapyrroles. Here, analysis and structure elucidation of the chlorophyll breakdown products in leaves of banana ( Musa acuminata) is reported. In senescent leaves of this monocot all chlorophyll catabolites identified were hypermodified fluorescent chlorophyll catabolites ( hmFCCs). Surprisingly, nonfluorescent chlorophyll catabolites (NCCs) were not found, the often abundant and apparently typical final chlorophyll breakdown products in senescent leaves. As a rule, FCCs exist only fleetingly, and they isomerize rapidly to NCCs in the senescent plant cell. Amazingly, in the leaves of banana plants, persistent hmFCCs were identified that accounted for about 80 % of the chlorophyll broken down, and yellow leaves of M. acuminata display a strong blue luminescence. The structures of eight hmFCCs from banana leaves were analyzed by spectroscopic means. The massive accumulation of the hmFCCs in banana leaves, and their functional group characteristics, indicate a chlorophyll breakdown path, the downstream transformations of which are entirely reprogrammed towards the generation of persistent and blue fluorescent FCCs. As expressed earlier in related studies, the present findings call for attention, as to still elusive biological roles of these linear tetrapyrroles.

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          Biliverdin reductase: a major physiologic cytoprotectant.

          Bilirubin, an abundant pigment that causes jaundice, has long lacked any clear physiologic role. It arises from enzymatic reduction by biliverdin reductase of biliverdin, a product of heme oxygenase activity. Bilirubin is a potent antioxidant that we show can protect cells from a 10,000-fold excess of H2O2. We report that bilirubin is a major physiologic antioxidant cytoprotectant. Thus, cellular depletion of bilirubin by RNA interference markedly augments tissue levels of reactive oxygen species and causes apoptotic cell death. Depletion of glutathione, generally regarded as a physiologic antioxidant cytoprotectant, elicits lesser increases in reactive oxygen species and cell death. The potent physiologic antioxidant actions of bilirubin reflect an amplification cycle whereby bilirubin, acting as an antioxidant, is itself oxidized to biliverdin and then recycled by biliverdin reductase back to bilirubin. This redox cycle may constitute the principal physiologic function of bilirubin.
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            Chlorophyll degradation during senescence.

            The catabolic pathway of chlorophyll (Chl) during senescence and fruit ripening leads to the accumulation of colorless breakdown products (NCCs). This review updates an earlier review on Chl breakdown published here in 1999 ( 69 ). It summarizes recent advances in the biochemical reactions of the pathway and describes the characterization of new NCCs and their formation inside the vacuole. Furthermore, I focus on the recent molecular identification of three chl catabolic enzymes, chlorophyllase, pheophorbide a oxygenase (PAO), and red Chl catabolite reductase (RCCR). The analysis of Chl catabolic mutants demonstrates the importance of Chl breakdown for plant development and survival. Mutants defective in PAO or RCCR develop a lesion mimic phenotype, due to the accumulation of breakdown intermediates. Thus, Chl breakdown is a prerequisite to detoxify the potentially phototoxic pigment within the vacuoles in order to permit the remobilization of nitrogen from Chl-binding proteins to proceed during senescence.
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              Chlorophyll breakdown in higher plants.

              Chlorophyll breakdown is an important catabolic process of leaf senescence and fruit ripening. Structure elucidation of colorless linear tetrapyrroles as (final) breakdown products of chlorophyll was crucial for the recent delineation of a chlorophyll breakdown pathway which is highly conserved in land plants. Pheophorbide a oxygenase is the key enzyme responsible for opening of the chlorin macrocycle of pheophorbide a characteristic to all further breakdown products. Degradation of chlorophyll was rationalized by the need of a senescing cell to detoxify the potentially phototoxic pigment, yet recent investigations in leaves and fruits indicate that chlorophyll catabolites could have physiological roles. This review updates structural information of chlorophyll catabolites and the biochemical reactions involved in their formation, and discusses the significance of chlorophyll breakdown. This article is part of a Special Issue entitled: Regulation of Electron Transport in Chloroplasts. Copyright © 2010 Elsevier B.V. All rights reserved.
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                Author and article information

                Journal
                Chemistry
                Chemistry
                chem
                Chemistry (Weinheim an Der Bergstrasse, Germany)
                WILEY-VCH Verlag (Weinheim )
                0947-6539
                1521-3765
                09 September 2013
                14 August 2013
                : 19
                : 37
                : 12294-12305
                Affiliations
                [[a] ]Institute of Organic Chemistry & Center for Molecular Biosciences, University of Innsbruck 6020 Innsbruck (Austria) E-mail: Bernhard.kraeutler@ 123456uibk.ac.at
                Author notes
                [[b]]

                Present address: Institut für Chemie, FG Organische Chemie, Technical University of Berlin, 10623 Berlin (Germany)

                Article
                10.1002/chem.201301907
                3814416
                23946204
                0cedd07b-443e-40b7-8f51-d815e92b7d4c
                © 2013 The Authors. Published by Wiley-VCH Verlag GmbH & Co. KGaA. This is an open access article under the terms of the Creative Commons Attribution Non-Commercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 17 May 2013
                Categories
                Full Papers

                Chemistry
                biosynthesis,chlorophyll,fluorescence,structures,tetrapyrroles
                Chemistry
                biosynthesis, chlorophyll, fluorescence, structures, tetrapyrroles

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