Novel Types of Phyllobilins in a Fern ‐ Molecular Reporters of the Evolution of Chlorophyll Breakdown in the Paleozoic Era

Abstract

AbstractBreakdown of chlorophyll (Chl), as studied in angiosperms, follows the pheophorbide a oxygenase/phyllobilin (PaO/PB) pathway, furnishing linear tetrapyrroles, named phyllobilins (PBs). In an investigation with fern leaves we have discovered iso‐phyllobilanones (iPBs) with an intriguingly rearranged and oxidized carbon skeleton. We report here a key second group of iPBs from the fern and on their structure analysis. Previously, these additional Chl‐catabolites escaped their characterization, since they exist in aqueous media as mixtures of equilibrating isomers. However, their chemical dehydration furnished stable iPB‐derivatives that allowed the delineation of the enigmatic structures and chemistry of the original natural catabolites. The structures of all fern‐iPBs reflect the early core steps of a PaO/PB‐type pathway and the PB‐to‐iPB carbon skeleton rearrangement. A striking further degradative chemical ring‐cleavage was observed, proposed to consume singlet molecular oxygen (1O2). Hence, Chl‐catabolites may play a novel active role in detoxifying cellular 1O2. The critical deviations from the PaO/PB pathway, found in the fern, reflect evolutionary developments of Chl‐breakdown in the green plants in the Paleozoic era.