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Review
. 2016 Apr 11;55(16):4882-907.
doi: 10.1002/anie.201508928. Epub 2016 Feb 26.

Breakdown of Chlorophyll in Higher Plants--Phyllobilins as Abundant, Yet Hardly Visible Signs of Ripening, Senescence, and Cell Death

Bernhard Kräutler  1
Affiliations
Review

Breakdown of Chlorophyll in Higher Plants--Phyllobilins as Abundant, Yet Hardly Visible Signs of Ripening, Senescence, and Cell Death

Bernhard Kräutler. Angew Chem Int Ed Engl. .

Abstract

Fall colors have always been fascinating and are still a remarkably puzzling phenomenon associated with the breakdown of chlorophyll (Chl) in leaves. As discovered in recent years, nongreen bilin-type Chl catabolites are generated, which are known as the phyllobilins. Collaborative chemical-biological efforts have led to the elucidation of the key Chl-breakdown processes in senescent leaves and in ripening fruit. Colorless and largely photoinactive phyllobilins are rapidly produced from Chl, apparently primarily as part of a detoxification program. However, fluorescent Chl catabolites accumulate in some senescent leaves and in peels of ripe bananas and induce a striking blue glow. The structural features, chemical properties, and abundance of the phyllobilins in the biosphere suggest biological roles, which still remain to be elucidated.

Keywords: biodegradation; chlorophyll; metabolism; natural product; plants.

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Figures

Figure 1
Figure 1
“Rusty pigment 14” from senescent leaves of barley (Hordeum vulgare), later named Hv‐NCC‐1 (1), was identified as the first nongreen Chl catabolite.8a
Figure 2
Figure 2
Phyllobilane (I),10 the name‐giving structure, depicted in two representative formulas to highlight its pseudocyclic (left) and extended conformations (right).
Figure 3
Figure 3
NCCs detected in naturally senescent cotyledons of Brassica napus (Bn‐NCCs 2–4)23 depicted in representative formulas to highlight its pseudocyclic (left) and extended conformations (right).
Figure 4
Figure 4
A simplified topographical model of Chl breakdown in a leaf cell, with relevant organelles and key types of Chl catabolites depicted.
Figure 5
Figure 5
Early steps of Chl breakdown in the chloroplasts produce pheophorbide a (Pheo a).
Figure 6
Figure 6
Photooxidation of the CdII‐pheophorbidate II and reduction of the 4,5‐dioxosecophytoporphyrin III furnishes RCC (7) via its methyl ester precursor 7‐Me.42
Figure 7
Figure 7
Chl breakdown from Pheo a via RCC (7) to primary FCCs (6/epi ‐6) is catalyzed by Pheo a oxygenase (PaO) and by two classes of RCC reductases (RCCR‐1 and RCCR‐2).9c
Figure 8
Figure 8
UV spectra of representative colorless phyllobilins of type‐I (FCC and NCC) and of type‐II (DFCC and DNCC).26a
Figure 9
Figure 9
Bio‐inspired partial chemical synthesis of the NCCs 5 and epi ‐5 by electrochemical reduction of RCC (7) to pFCC and epi‐pFCC (6 and epi ‐6), followed by stereoselective acid‐catalyzed isomerization to 5 and epi ‐5.20b
Figure 10
Figure 10
Structural formulas (left) of DNCCs 8 a/8 b (from barley)57 and ent ‐8 a (from a Norway maple leaf),58 whose CD and UV spectra (right) feature the properties of an intriguing enantiomer of 8 a.
Figure 11
Figure 11
Branching of Chl breakdown occurs at the level of FCCs and provides pathways to downstream type‐I and type‐II phyllobilins (see Tables 1–3 for examples of R1, R2, and R3).10
Figure 12
Figure 12
Constitutional formulas of two common natural NCCs. Catabolites epi ‐11 and epi ‐9 (first identified as Cj‐NCC‐1 and Nr‐NCC‐2, respectively), which are also present in the peels of apples and pears (see Table 1).
Figure 13
Figure 13
Generalized NCC formula, including atom numbering (top left) and structural formulas of natural NCCs with unique structures: doubly glycosylated Pd‐NCC‐32 (epi ‐18), bicycloglycosidic Ug‐NCC‐3 (19), and epimeric NCC esters epi ‐20/epi‐21 from banana peels (R=daucyl unit, Mc‐NCC‐58 has an R configuration at C10, Mc‐NCC‐55 is the S epimer).
Figure 14
Figure 14
Acid‐induced isomerization of methyl esters of primary FCCs (6‐Me/epi ‐6‐Me) to NCCs is slow and lacks significant stereoselectivity; it furnishes methyl esters of their normal and epi lineages 5‐Me/epi ‐5‐Me, as well as of both of their enantiomers (ent‐5‐Me/ent‐epi‐5‐Me).20b
Figure 15
Figure 15
Structures of hypothetical modified FCCs (mFCCs, right) are frequently extrapolated from those of the corresponding isomeric NCCs (left).
Figure 16
Figure 16
Top: Structural formulas of hmFCCs from leaves of bananas (Ma‐FCCs) and of Sp. wallisii (Sw‐FCC‐62), and reproduction (bottom) of a cover picture depicting a yellow banana leaf when observed under daylight or under black light.28b
Figure 17
Figure 17
Generalized formulas of colorless and nonfluorescent type‐II phyllobilins: DNCCs, 4‐hydroxymethyl‐DNCCs and 2‐hydroxymethyl‐iso‐DNCCs.26
Figure 18
Figure 18
Top: Deformylation of 32‐OH‐pFCC by CYP89A9 is proposed as an entry to type‐II phyllobilins by furnishing the hypothetical DFCC 35; ester hydrolysis by MES16 produces DFCC 34 (At‐DFCC‐33), which isomerizes to DNCC 30 (At‐DNCC‐33).26c Bottom: Abridged outline of a possible mechanism (depicted by ring A) of the deformylation of FCC 21 to DFCC 35, catalyzed by the cytochrome P450 enzyme CYP89A9.26a
Figure 19
Figure 19
Phyllobilins lacking a 32‐OH group are directly derived from pFCC (6). In vivo deformylation of pFCC(6) in A. thaliana by CYP89A9 (CYP) and hydrolysis by the methyl esterase MES16 (MES) is a pathway to three types of nonfluorescent DCCs (right: the genuine DNCCs 31 a/31 b, 2HM‐iso‐DNCC 35, 4HM‐DNCC 37), proposed to be formed by isomerization of the corresponding hypothetical fluorescent DCCs with R=H (center: 84H‐pDFCC, 84H‐2HM‐iso‐DFCC, and 84H‐4HM‐DFCC).26b
Figure 20
Figure 20
Overview of Chl breakdown in leaves of A. thaliana (wild type). The proposed major pathway, from Chl a to At‐DNCC‐33,26c is marked with bold arrows (CYP=CYP89A9, MES=MES16, Gls=putative glycosidase; see Figure 19 for the structures of type‐II phyllobilins derived from pFCC).
Figure 21
Figure 21
Ripening fruit (left) and degreening florets of broccoli (right) undergo Chl breakdown and accumulate colorless phyllobilins.59, 61
Figure 22
Figure 22
Top: Yellow ripe bananas show a blue luminescence. When yellow bananas are illuminated with UV light (black light), a blue glow of the bananas originates from the abundant FCCs and can be seen by the naked eye86 (picture taken from Ref. 28a). Bottom: Major hmFCCs from banana peels are FCC daucyl esters.28a, 85
Figure 23
Figure 23
hmFCCs and NCCs are generated in the peels of ripening bananas, thereby indicating a pathway of Chl breakdown that is split at the stage of 32‐OH‐epi‐pFCC (epi ‐23).51
Figure 24
Figure 24
Structural formulas of yellow Chl catabolites (YCCs) and pink Chl catabolites (PiCCs), which may contribute to the color of senescent leaves of deciduous trees.89
Figure 25
Figure 25
The NCCs 11 and epi ‐11 are oxidized by an extract from Sp. wallisii leaves to epimeric 15‐OH‐NCCs, which are dehydrated in weak acid to furnish the YCC 46Z.91
Figure 26
Figure 26
Top: Oxidation of YCC 46Z in the presence of ZnII ions furnishes the blue ZnII complex Zn‐47, from which the PiCC 47 is liberated by treatment with acid or phosphate; bottom: molecular structure of the PiCC 47 as deduced from X‐ray crystal structure analysis (C gray, green H, red O, blue N; left: top view, right: side view).94a
Figure 27
Figure 27
UV/Vis spectra (—, left axis) and fluorescence emission spectra (‐ ‐ ‐ ‐, right axis) of NCC epi ‐11 (top) and of the phyllochromobilins 46Z (a YCC) and 47 (a PiCC), as well as of the blue ZnII complex Zn‐47.94
Figure 28
Figure 28
Complexation of transition‐metal ions by PiCC 47 restructures the ligand to a Z/Z configuration and leads to blue metal complexes. Zn‐47 and Cd‐47 are complexes with closed‐shell metal ions, and exhibit strong red luminescence.94a
Figure 29
Figure 29
Binding of ZnII ions to the weakly luminescent YCC methyl ester 46Z‐Me furnishes the strongly fluorescent 2:1 complex Zn(46Z‐Me)2.94b,94c
Figure 30
Figure 30
Abbreviated general outline of the PaO/phyllobilin pathway in some higher plants.10, 11 Chl is broken down in a linear sequence from pheophorbide a (Pheo a) to primary FCCs (pFCCs). Branching out at the stage of FCCs gives several downstream lines of type‐I and type‐II phyllobilins. Colorless phyllobilins (NCCs and DNCCs) accumulate in senescent and ripening plant tissues. The colorless and nonfluorescent NCCs and DNCCs may be oxidized further to yellow (and then pink) phyllochromobilins.
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References

    1. None
    1. Kräutler B., Matile P., Acc. Chem. Res. 1999, 32, 35–43;
    1. Morel A. in Chlorophylls and Bacteriochlorophylls. Biochemistry Biophysics, Functions and Applications (Eds.: B. Grimm, R. Porra, W. Rüdiger, H. Scheer), Adv. Photosynth. Res., Vol. 25, Springer, Dordrecht, 2006, S. 521–534.
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