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Biosynthesis of Food Constituents: Natural Pigments. Part 1 – a Review

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Biosynthesis of Food Constituents: Natural Pigments. Part 1 – a Review Czech J. Food Sci. Vol. 25, No. 6: 291–315 Biosynthesis of Food Constituents: Natural Pigments. Part 1 – a Review Jan VELÍŠEK, Jiří DAVÍDEK and Karel CEJPEK Department of Food Chemistry and Analysis, Faculty of Food and Biochemical Technology, Institute of Chemical Technology in Prague, Prague, Czech Republic Abstract VELÍŠEK J., DAVÍDEK J., CEJPEK K. (2007): Biosynthesis of food constituents: Natural pigments. Part 1 – a re- view. Czech J. Food Sci., 25: 291–315. This review article gives a survey of the generally accepted biosynthetic pathways that lead to the most important natural pigments in organisms closely related to foods and feeds. The biosynthetic pathways leading to hemes, chlo- rophylls, melanins, betalains, and quinones are described using the enzymes involved and the reaction schemes with detailed mechanisms. Keywords: biosynthesis; tetrapyrroles; hemes; chlorophylls; eumelanins; pheomelanins; allomelanins; betalains; betax- anthins; betacyanins; benzoquinones; naphthoquinones; anthraquinones Natural pigments are coloured substances syn- noids. Despite their varied structures, all of them thesised, accumulated in or excreted from living are synthesised by only a few biochemical path- or dying cells. The pigments occurring in food ways. There are also groups of pigments that defy materials become part of food, some other pig- simple classification and pigments that are rare ments have been widely used in the preparation or limited in occurrence. of foods and beverages as colorants for centuries. Many foods also owe their colours to pigments that 1 TETRAPYRROLES form in food materials and foods during storage and processing as a result of reactions between food Tetrapyrroles (tetrapyrrole pigments) represent a constituents, notably the non-enzymatic browning relatively small group of pigments that contribute reaction and the Maillard reaction. Furthermore, the greatest range of colours and are, at the same many artificial colorants have been used to improve time, the most abundant globally. All are based on the colour of foods. the same structure in which the pyrrole-derived Almost all biological pigment structures can rings A, B, C, and D (Figure 1) are joined into be reduced to no more than a few major classes. tetrapyrrole by one-carbon unit links (methine The most important chromophores of biological bridges) between the pyrrole rings α position pro- pigments are N-heterocyclic compounds, O-hete- viding a chromophore with a system of conjugated rocyclic compounds, quinones, and tetraterpe- double bonds. Tetrapyrroles occur either in their Partly supported by the Ministry of Education, Youth and Sports of the Czech Republic (Project No. MSM 6046137305). 291 Vol. 25, No. 6: 291–315 Czech J. Food Sci. 5 7 3 5 7 3 4 6 4 6 8 2 A B 8 2 A B NN 1 NH N 9 1 H 9 2 3 7 8 12 13 17 18 21 22 10 20 10 20 24 23 A B 19 11 1 C D 19 19 11 N HN 6 N H N N 4 N 9 11 N 14 16 N 18 D C 12 18 14 C 12 5 10 15 D H 16 13 17 16 14 13 17 15 E 15 2 1 13 13 basic structure of bilins basic structure of porphyrins basic structure of chlorophylls Figure 1 linear form (sometimes bound to sugars), which are of the tetrapyrrole molecule itself and relatively known as bile pigments or bilins or in the cyclic little by the metal (Gross 1987, 1991; Hendry & forms based on a macrocyclic tetrapyrrole, which Houghton 1992). is known as porphyrin1 (IUPAC 2007). The tetrapyrroles are mostly classified according 1.1 Porphyrins to their occurrence in nature. The linear bilins com- prise two groups of pigments, phycobilins and bile The biosynthesis of porphyrins requires the pigments. The first group comprises the pigments availability of a suitable amino acids and its con- of some algae, the second group are the typical stituent nitrogen to yield the building block of pigments of animal urine and faeces (formed by all tetrapyrroles in nature. This building block, the breakdown of heme pigments). The porphyrin 5-aminolevulinic (δ-aminolevulinic or 5-ami- based pigments constitute the chromophore of no-4-oxopentanoic) acid is sinthesised via a dif- two most important metalloproteins, i.e. red heme ferent pathway in animal cells, lower plants, and pigments (hemes) chelated with iron, and green bacteria that in green plants. chlorophyll pigments (chlorophylls) chelated with In animal cells, 5-aminolevulinic acid biosyn- magnesium2. The basic structure (IUPAC 2007) of thesis involves two steps. The first step is the the majority of chlorophylls represents the cyclic biosynthesis of succinyl-CoA from succinic acid tetrapyrrole, i.e. 17,18-dihydroporphyrin, with and HS-CoA under the catalysis of succinyl coen- partially reduced ring D and the fifth ring (ring E) zyme A synthetase (ADP forming, also known as formed by cyclisation of one of the propionic succinate thiokinase, EC 6.2.1.5). The second step acid side chains attached at C-13 (Figure 1). The is the condensation of glycine with succinyl-CoA colour of the particular cyclic tetrapyrrole is de- to l-2-amino-3-oxoadipic acid by the pyridoxal termined largely by the structure and substitutions phosphate-containing enzyme 5-aminolevulinate 1The 1–24 numbering system upon which the numbering system for corrinoids is based was adopted for the porphyrin nucleus shown in Figure 1. The 2,3,7,8,12,13,17, and 18 positions have commonly been referred to generically as β-positions (i.e. of the pyrrole rings). Similarly, positions at 1,4,6,9,11,14,16, and 19 have been referred to generically as α-positions, while those at 5,10,15, and 20 are referred to generically as meso-positions (IUPAC 2007). 2Aside from its importance as the prosthetic group of hemoglobin (the respiratory pigment in red blood cells of ver- tebrates) and myoglobin (the pigment in muscle fibers), hemes are also the prosthetic groups of a small number of enzymes, such as detoxifying cytochromes and cytochromes (Voet & Voet 1990). Chlorophylls are found in most plants, algae, and cyanobacteria. Their molecules in Eucaryota are specifically arranged in and around pigment protein complexes called photosystems, which are embedded in the thylakoid membranes of chloroplasts. Thylakoid membranes are a phospholipid bilayer membrane-bound compartment internal to chloro- plasts, and represent the majority of its internal structure. Chloroplasts like all other plastids (including chromoplasts and leucoplasts), are organelles found in the photosynthetic eukaryotic species. Chromoplasts are responsible for the pigment synthesis and storage, they mainly store carotenoids but also other pigments. In chloroplasts, some carotenoids are also used as accessory pigments in photosynthesis. Leucoplasts are non-pigmented and predictably located in roots and non-photosynthetic tissues of plants. They may become specialised for bulk storage of starch, lipid or protein and are then known as amyloplasts, elaioplasts, or proteinoplasts, respectively (Gross 1987, 1991; Hendry & Houghton 1992). 292 Czech J. Food Sci. Vol. 25, No. 6: 291–315 HOOC COOH succinic acid HS-CoA + ATP EC 6.2.1.5 ADP + P HS CoA CO2 O O O HOOC + CoA HOOC H2N S COOH COOH COOH NH2 EC 2.3.1.37 EC 2.3.1.37 NH2 glycine succinyl-CoA L-2-amino-3-oxoadipic acid 5-aminolevulinic acid Figure 2 synthase (EC 2.3.1.37) (Figure 2). l-2-Amino-3-oxo- acid to transfer RNA (tRNAGlu). In the second adipic acid eliminates carbon dioxide and yields reaction, the glutamyl-tRNA complex is converted 5-aminolevulinic acid, which is then exported to to a glutamic acid 1-semialdehyde by glutamate- cytoplasm for further metabolism (IUBMB 2007; tRNA reductase (EC 1.2.1.70). Using pyridoxamine Bergfeld et al. 2003). 5'-phosphate as a cofactor, glutamate 1-semialde- In green plants, 5-aminolevulinic acid is formed hyde 2,1-aminomutase (glutamate semialdehyde from l-glutamic acid in three reactions (Figure 3). aminotransferase, EC 5.4.3.8) converts glutamic In the first reaction, glutamate-tRNA ligase acid 1-semialdehyde to 5-aminolevulinic acid via (EC 6.1.1.17) catalyses the ligation of glutamic 4,5-diaminopentanoic acid (IUBMB 2007). Glu Glu NADP + tRNA ATP + tRNA AM P +PP NADPH + H O O HOOC HOOC HOOC COOH tRNA H EC 1.2.1.70 NH NH2 2 NH2 EC 6.1.1.7 Glu L-glutamic acid 1-semialdehyde L-glutamic acid Glu-tRNA H2N EC 5.4.3.8 OH NH 2 NH2 NH2 PO H HOOC HOOC HOOC N CH3 HN HN HN H pyridoxamine-5´-phosphate (bound non-covalently OH OH OH to the enzyme) PO PO PO NCH 3 N CH3 N CH3 H H H O NH2 H N H2N 2 COOH COOH 4,5-diaminopentanoic acid 5-aminolevulinic acid COOH COOH COOH H N H2N H2N 2 H HN HN HN H HN OH OH OH OH PO PO PO PO NCH NCH 3 NCH3 N CH3 3 H H H H pyridoxal 5´-phosphate (bound as an aldimine to a Lys residue of the enzyme) Figure 3 293 Vol. 25, No. 6: 291–315 Czech J. Food Sci. The next three steps of porphyrin biosynthesis In the pathway leading to porphyrins, uropor- follow those of vitamin B12 coenzyme (adenosylco- phyrinogen decarboxylase (uroporphyrinogen balamin) pathway. These steps (Figure 4) start with decarboxylase, EC 4.1.1.37) catalyses decarboxyla- the condensation of two 5-aminolevulinic acids tion of the acetic acid residues attached to C-2, to form porphobilinogen (aminolevulinate dehy- C-7, C-12, and C-18 of uroporphyrinogen III to dratase or porphobilinogen synthase, EC 4.2.1.24), yield coproporphyrinogen III also known as copro- four porphobilinogens are converted to hy- gen III (Figure 4).
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