Chlorophyll Breakdown – How Chemistry Has Helped to Decipher a Striking Biological Enigma

Abstract

How the fall colors arise and how chlorophyll (Chl) breakdown occurs in higher plants has remained enigmatic until three decades ago. Fundamental insights into this fascinating puzzle have been gained, meanwhile, by basic contributions from plant biology and chemistry. This short review is a personal account of key advances from synthetic, mechanistic, and structural chemistry that led to the discovery of the bilin-type Chl catabolites and helped elucidate the metabolic processes that generated them from Chl.1 Introduction2 Discovery and Structure Elucidation of a First Non-Green Chl Catabolite3 Structure Elucidation of Fleetingly Existent Blue-Fluorescent Chl Catabolites4 The Red Chl Catabolite – Key Ring-Opened Tetrapyrrole Accessed by Partial Synthesis5 Synthesis of ‘Primary’ Fluorescent Chl Catabolites by Reduction of Red Chl Catabolite6 Nonfluorescent Chl Catabolites from Isomerization of Fluorescent Chl Catabolites7 Persistent Fluorescent Chl Catabolites and Blue-Luminescent Bananas8 Discovery, Structure Elucidation, and Biological Formation of Dioxobilin-Type Chl Catabolites9 Occurrence, Partial Synthesis, and Structure of Phyllochromobilins, the Colored Bilin-Type Chl Catabolites10 Conclusion and Outlook

In Search of Bioactivity – Phyllobilins, an Unexplored Class of Abundant Heterocyclic Plant Metabolites from Breakdown of Chlorophyll

“…The possible correlations between the phylogenetic relationship of plant species and the pattern of ‘their PBs’, has, so far, remained unsolved, but is another potentially interesting issue from the pharmacological point of view. Aside of the natural PBs, as lead structures, synthetic modifications may enlarge the array of these bilin‐type compounds . With the number of structurally identified natural PBs growing steadily, correlations between botanical families and the PBs they contain may be established, and, in return, predictions about the expected PB contents of a certain plant may become possible.…”

“…Aside of the natural PBs, as lead structures, synthetic modifications may enlarge the array of these bilintype compounds. [75] With the number of structurally identified natural PBs growing steadily, correlations between botanical families and the PBs they contain may be established, and, in return, predictions about the expected PB contents of a certain plant may become possible. With regards to the potential bioactivities of PBs, such as antioxidant activity, and the occurrence of PBs in food in varying amounts, as demonstrated for apples and pears, it might be of interest to identify fruit and vegetables with a high PB contents, which may contribute to the health benefits of a plant based diet.…”

Chlorophyll breakdown—Regulation, biochemistry and phyllobilins as its products

“…Pheophorbide a (Pheide a) has been identified as the ultimate intermediate with an intact porphyrinoid macrocycle (see Scheme 2 and later sections of this chapter) (Hörtensteiner, 2013). The specific oxygen-dependent cleavage of the macrocycle of Pheide a by Pheide a oxygenase (PAO) generates the 'red Chl catabolite' (RCC) (Kräutler, 2019;Kräutler, Mühlecker, Anderl, & Gerlach, 1997;Rodoni et al, 1997a), a cryptic red formyloxo-bilin that represents the common precursor of the natural Chl-derived PBs in angiosperms (Hörtensteiner, Wüthrich, Matile, Ongania, & Kräutler, 1998;Pružinská, Anders, Tanner, Roca, & Hörtensteiner, 2003). Efficient enzymatic reduction (in a form of 'metabolic chanelling') of RCC by RCC reductases (RCCRs) (Rodoni, Vicentini, Schellenberg, Matile, & Hörtensteiner, 1997b;Sugishima, Kitamori, Noguchi, Kohchi, & Fukuyama, 2009;Wüthrich, Bovet, Hunziker, Donnison, & Hörtensteiner, 2000) next produces a first type of a fluorescent formyloxobilin (fluorescent type-I PB), the 'primary' fluorescent Chl catabolites (pFCCs).…”

“…Hence, the pFCCs are produced in one of two C16-epimeric forms by the stereospecific reduction of the C15=C16 double bond of RCC by one of two lines of cofactor-free RCCRs, establishing the deep rooted relevance of two stereo-types of RCCRs (Hörtensteiner et al, 2000). An electrochemical reduction process modeled a stereounspecific version of RCC reduction by the RCCRs (Kräutler, 2019;Oberhuber et al, 2008). Typical FCCs, now also classified as fluorescent type-I PBs (Kräutler, 2016), do not accumulate in plant cells and disappear quickly, either by rapid isomerization to corresponding NCCs (in the weakly acidic medium of the vacuoles, in particular) (Christ et al, 2012;Oberhuber et al, 2003;Oberhuber et al, 2008), or by deformylation to corresponding DFCCs on the way to type-II PBs (Christ et al, 2013;Hörtensteiner & Kräutler, 2011).…”

A pink colored dioxobilin-type phyllobilin from breakdown of chlorophyll

“…Colorless PBs accumulate in senescent leaves as products of the largely common 'PAO/phyllobilin' pathway of Chl breakdown [6][7][8]. They derive from a 'red Chl catabolite' (RCC) [9][10][11], the cryptic red formyloxobilin that results from specific oxygenolysis of the macrocycle of pheophorbide a (Pheide a) by Pheide a oxygenase (PAO), as the common progenitor of the PBs (see Fig. 1) [12,13].…”