Abstract
The disappearance of chlorophyll is a visual sign of fruit ripening. Yet, chlorophyll breakdown in fruit has hardly been explored; its non-green degradation products are largely unknown. Here we report the analysis and structure elucidation of colorless tetrapyrrolic chlorophyll breakdown products in commercially available, ripening bananas (Musa acuminata, Cavendish cultivar). In banana peels, chlorophyll catabolites were found in an unprecedented structural richness: a variety of new fluorescent chlorophyll catabolites (FCCs) and nonfluorescent chlorophyll catabolites (NCCs) were detected. As a rule, FCCs exist only "fleetingly" and are hard to observe. However, in bananas several of the FCCs (named Mc-FCCs) were persistent and carried an ester function at the propionate side-chain. NCCs were less abundant, and exhibited a free propionic acid group, but functional modifications elsewhere. The modifications of NCCs in banana peels were similar to those found in NCCs from senescent leaves. They are presumed to be introduced by enzymatic transformations at the stage of the mostly unobserved, direct FCC-precursors. The observed divergent functional group characteristics of the Mc-FCCs versus those of the Mc-NCCs indicated two major "late" processing lines of chlorophyll breakdown in ripening bananas. The "last common precursor" at the branching point to either the persistent FCCs, or towards the NCCs, was identified as a temporarily abundant "secondary" FCC. The existence of two "downstream" branches of chlorophyll breakdown in banana peels, and the striking accumulation of persistent Mc-FCCs call for attention as to the still-elusive biological roles of the resulting colorless linear tetrapyrroles.
Highlights
Breakdown of chlorophyll is a major contributor to the diagnostic color changes in fall leaves.[1]
A breakthrough in this area was provided by the identification and structure elucidation of a colorless tetrapyrrole in senescent leaves of barley (Hordeum vulgare), named Hv-nonfluorescent chlorophyll catabolites (NCCs)-1.[1,8] identification of the structures of relevant chlorophyll catabolites,[9,10] of key enzymes and their genes,[11,12,13] has resulted in general insights into the basic processes involved in chlorophyll breakdown in higher plants.[13,14]
One of them was proposed to proceed through the so-called “Type I” degradation path leading to modified-green chlorophylls, whereas non-green catabolites were not identified in that study.[23]
Summary
In spite of broad research efforts, the “disappearance” of chlorophyll was a biological puzzle for a long time,[6] since its products remained concealed.[7] a breakthrough in this area was provided by the identification and structure elucidation of a colorless tetrapyrrole in senescent leaves of barley (Hordeum vulgare), named Hv-NCC-1.[1,8] identification of the structures of relevant chlorophyll catabolites,[9,10] of key enzymes and their genes,[11,12,13] has resulted in general insights into the basic processes involved in chlorophyll breakdown in higher plants.[13,14] Colorless “nonfluorescent chlorophyll catabolites” (NCCs) are typically found (to accumulate) in senescent leaves and have been suggested to represent (with notable exceptions[15,16,17,18,19]) the “final stage” of chlorophyll breakdown (see Figure 1).[13] Likewise, ripening apples and pears contained known NCCs, suggesting a “common path” of chlorophyll breakdown in leaf senescence and fruit ripening.[5,20] Surprisingly, in (the peels of) ripening bananas (Musa acuminata, Cavendish cultivar) chlorophylls fade to give fluorescent chlorophyll catabolites (FCCs) mainly, and yellow bananas glow blue, when analyzed under UV light.[21,22]. We have identified most of these catabolites, as well as their structures and their changing occurrence during the ripening process, as reported here
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