Pyro-Phyllobilins: Elusive Chlorophyll Catabolites Lacking a Critical Carboxylate Function of the Natural Chlorophylls.

Chengjie Li,Bernhard Kräutler,Joachim Berghold,Klaus R Liedl,Klaus Wurst,Maren Podewitz

doi:10.1002/chem.201705331

Abstract

A β‐keto ester grouping is a characteristic of ring E of the chlorophylls (Chls). Its presence has also reinforced the original identification of nonfluorescent Chl catabolites (NCCs) as colorless, amphiphilic phyllobilins (PBs). Polar NCCs were also detected in higher plants, in which a free carboxyl group replaced the ring E ester group. Such NCCs are surprisingly resistant to loss of this carboxyl unit, and NCCs lacking the latter, that is, pyro‐NCCs (pyNCCs), have not been reported. Intrigued by the question of the natural occurrence of pyro‐phyllobilins (pyPBs), we have prepared a representative pyNCC by decarboxylation of a natural NCC. We also converted the pyNCC into its yellow oxidation product, a pyro‐YCC (pyYCC). The solution structures of pyNCC and of pyYCC, and a crystal structure of the pyYCC methyl ester (pyYCC‐Me) were obtained. pyYCC‐Me features the same remarkable H‐bonded and π‐stacked dimer structure as the corresponding natural yellow Chl catabolite (YCC) with the ring E methyl ester group. Indeed, the latter substituent has little effect on the structure, as well as on the unique self‐assembly and photoswitch behavior of yellow PBs.

Highlights

In higher plants chlorophyll (Chl) breakdown[1,2] produces bilintype linear tetrapyrroles, named phyllobilins (PBs).[3–5] The PBs have a similar structure to the ubiquitous heme-derived bilins.[6,7] PBs carry a characteristically substituted “extra” cyclopentanone moiety, derived from ring E of Chl.[3,5] PBs are congested at their “southern” meso-position, a source, probably, of extra reactivity and of unusual conformational control,[8] as is found in highly substituted porphyrin(oid)s.[9,10] The Chl-derived methyl ester group at ring E of natural PBs affects their properties and may be relevant to their possible biological functions
The natural formation of PBs from Chls implies an oxidative opening at the “northern” (a) meso-position of the macrocycle.[11,12]. This key step is achieved by pheophorbide a oxygenase (PaO), which degrades pheophorbide a (Pheo a) to the red Chl catabolite (RCC).[11–13]
We report here 1) the partial synthesis of the pyro-type nonfluorescent Chl catabolites (NCCs) 3 from NCC 1, 2) oxidation of 3 to the yellow pyro-type yellow Chl catabolites (YCCs) 4, and 3) structural, spectroscopic, and photochemical properties of these novel pyPBs

Summary

Introduction

The natural formation of PBs from Chls implies an oxidative opening at the “northern” (a) meso-position of the macrocycle.[11,12] This key step is achieved by pheophorbide a oxygenase (PaO), which degrades pheophorbide a (Pheo a) to the red Chl catabolite (RCC).[11–13]. In extracts of the green alga Chlamydomonas reinhardtii[19,20] pyro-pheophorbide a (pyPheo a) was detected under anaerobic conditions, and a “decarboxymethylase” was suggested to be relevant in Chl breakdown in this alga (see Scheme 2) This product of an apparent loss of the entire methyl ester group of Pheo a may result from a two-step sequence via spontaneous decarboxylation of the first-formed 132-carboxyl-pyro-pheophorbide a.[21,22]. We report here 1) the partial synthesis of the pyro-type NCC (pyNCC) 3 from NCC 1, 2) oxidation of 3 to the yellow pyro-type YCC (pyYCC) 4, and 3) structural, spectroscopic, and photochemical properties of these novel pyPBs

Results and Discussion

Conclusions

Conflict of interest