Chemical and Antioxidant Properties of Betalains - American

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Chemical and Antioxidant Properties of Betalains Imen Belhadj Slimen,*,†,‡ Taha Najar,†,‡ and Manef Abderrabba‡ †

Department of Animal, Food and Halieutic Resources, National Agronomic Institute of Tunisia, 43 Avenue Charles Nicolle, 1082 Tunis, Tunisia ‡ Laboratory of Materials, Molecules and Applications, Preparatory Institute for Scientific and Technical Studies, BP 51, 2070 La Marsa, Tunis, Tunisia ABSTRACT: Betalains are vacuolar pigments composed of a nitrogenous core structure, betalamic acid. Betalamic acid condenses with imino compounds (cyclo-DOPA/its glucosyl derivates) or amino acids/derivates to form violet betacyanins and yellow betaxanthins. These pigments have gained the curiosity of scientific researchers in recent decades. Their importance was increased not only by market orientation toward natural colorants and antioxidants but also by their safety and health promoting properties. To date, about 78 betalains have been identified from plants of about 17 families. In this review, all of the identified pigments are presented, followed by a comprehensive discussion of their structure−activity relationship. KEYWORDS: betanin, indicaxanthin, caryophyllales, fluorescence, antioxidant activity

1. INTRODUCTION Betalains are water-soluble nitrogen-containing pigments, dissolved in the vacuolar sap as bis-anions.1 Betalains are considered as chemosystematic markers of the suborder Chenopodiniae within the Caryophyllales (except Caryophyllaceae and Molluginaceae, which accumulate anthocyanins instead), wherein they replace anthocyanins.2,3 Betalains are also detected in some genera of higher fungi such as the fly agaric Amanita muscaria, Hygrocybe, and Hygrophorus.4,5 In early days, betaxanthins were addressed erroneously as flavonoids and betacyanins were called “nitrogenous anthocyanins”. Both pigment types were addressed as betalains for the first time in 1968 by Mabry and Dreiding.6 The first betanin identified was betacyanin from red beet,7 and indicaxanthin from yellow-orange cactus pear was the first betaxanthin structurally characterized.8 Red beet has been considered for a long time as the unique source of betalains, which may justify the scarce attention toward these pigments. During the two past decades, promising new sources of betalains were reported, allowing broadening of the hitherto limited betalain perspectives as natural antioxidants and food colorants.9 Moreover, some plants producing betalains, such as Opuntia species, are easy to grow in arid/ dry lands. This implies a lower production cost, in addition to the use of these plants as a source of phytochemicals and ruminant feed after pigment extraction. In this overview, some features of betalain chemistry will be discussed.

Figure 1. Structure of betalamic acid (a), betaxanthins (b), and betacyanins (c).

derivates forms the yellow betaxanthins (Greek: xanthos = yellow) (Figure 1b,c). In general, betalains are stable between pH 3 and 7.10,11 Owing to their hydrophilic nature, betalains can be extracted using precooled water or aqueous methanol. Highly pigmented crops are recommended to maximize pigment yield. Once released from their protecting compartment, betalains are affected by multiple degrading factors such as pH, water activity, light, oxygen metal ions, temperature, and enzymatic reactions.10−12 Within the optimal range of pH stability,

2. CHEMISTRY 2.1. Isolation, Stabilization, and Optical Properties. Betalamic acid (Figure 1a) [4-(2-oxoethylidene)-1,2,3,4-tetrahydropyridine-2,6-dicarboxylic acid] is the core structure of all betalains. The condensation of betalamic acid with cyclo-DOPA [cyclo-L-(3,4-dihydroxyphenylalanine)] or its glucosyl derivates leads to the formation of violet betacyanins (Greek: kyaneos = blue), whereas its condensation with amino acids or their © XXXX American Chemical Society

Received: September 21, 2016 Revised: December 6, 2016 Accepted: January 6, 2017

A

DOI: 10.1021/acs.jafc.6b04208 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry Table 1. Fluorescence Properties of Some Betalain Pigments amino acid

λexc (nm)

λems (nm)

Stokes shift (nm)

MetSO Asp tyramine dopamine His Tyr Ala Met Leu Phe phenelethylamine ethylamine 1 propylamine 2 N-methylethanamine 4 N-methyl-N-propylamine 5 pyrrolidine 6 aniline 7 N-methylaniline 8 N-ethylaniline 9 indoline 10 (S)-indoline-2-carboxylic acid 12

535 463 464 466 463 474 475 474 464 465 465 474 463 464 464 464 473 472 472 472 472 471 513 494 494 521 529

608 515 509 508 510 550 509 507 506 512 509 509 508 509 509 510 551 548 548 548 550 549 560 553 554 570 575

73 52 45 42 47 76 34 33 42 47 44 35 45 45 45 46 78 76 76 76 78 78 47 59 60 49 46

betalain betanin indicaxanthin vulgaxanthin I vulgaxanthin II dopaxanthin miraxanthin I miraxanthin II miraxanthin III miraxanthin V muscaurin VII portulacaxanthin II alanine-Bx methionine-Bx vulgaxanthin IV phenylalanine-Bx phenelethylamine-Bx

Pro Gln Glu DOPA

ref 30 28, 28, 29 28, 24 29 29 29 28, 29 28, 29 29 29 29 24 24 24 24 24 24 24 24 24 24 24

29 29 29

29 29

betanin has significant fluorescence, lower than that of indicaxanthin. The authors reported an excitation peak at 535 nm and an emission peak at 608 nm. Moreover, it is known that fluorescence intensity is enhanced by carboxyl groups and reduced by electron donating groups such as aromatic ring and hydroxyl groups.24 In betacyanins, resonance is extended to the indole ring. Therefore, their fluorescence is weaker compared to betaxanthins. Interestingly, a strong Raman activity owing to fluorescence interference of betanin aromatic ring vibrations was reported for the first time by Sandquist and McHale,30 and it was consistent with previous findings showing the visible transition of betanin, betanidin, and gomphrenin from HOMO → LUMO excitation (HOMO and LUMO are acronyms for highest occupied molecular orbital and lowest unoccupied molecular orbital, respectively). This transition characterizes the lowest singlet excited states and indicates an emission of energy. The electron density moves from the aromatic ring to the tertahydropyridyl moiety.31 However, further investigations in betacyanin fluorescence are still needed. Fluorescence properties of some studied betalains are summarized in Table 1. Fluorescence is a very interesting nanoscale probe, since the fluorescence decay occurs on the nanosecond time scale. The emission of the fluorophore allows characterizing the changes in nanoenvironment, size of the molecules and their interactions, inter- and intramolecular distances, and molecular mixtures.32 Betalamic acid was confirmed to be the chromophore of all betalains, due to the presence of conjugated double bonds,10 and the chiral center is retained at C-6. Betacyanins exhibit a shift of absorbance maximum in water from 424 nm to 541 ± 9 nm, originating from the extension of electronic resonance of 1,7-diazaheptamethine system to the diphenolic aromatic ring

temperature will be the most decisive factor about betalain decomposition.20 Although betalain containing plants also contain endogenous ascorbic acid to protect the most labile compounds, several authors13−16 recommended the addition of ascorbic acid in the extraction medium since it leads to a slightly acidic pH, stabilizes betacyanins, and avoids the formation of quinones by the effect of polyphenol oxidases (PPOs).17 Isoascorbic acid was also reported to enhance betalains’ stability by oxygen removal.18,19 Moreover, chelating agents such as citric acid and EDTA were proven to be suitable for betalain stabilization, possibly by a partial neutralization of the electrophilic center of these pigments, through association around the positively charged amino nitrogen.19−21 Finally, ß-cyclodextrin and glucose oxidase contribute in betalain stabilization through adsorbing free water and removing dissolved oxygen, respectively.22,23 It is interesting to note herein that phenolic antioxidants and tocopherol did not show any stabilizing effect.18 Due to the conjugated dienes of the 1,7-diazaheptamethine structure, betalains exhibit absorption in both UV and visible regions.24 Structural implication on fluorescence of betaxanthins was reported.24,25 Betaxanthins are known as fluorescent pigments that are able to absorb and emit fluorescence within the visible area of the electromagnetic spectrum. The maximum excitation wavelengths measured for betaxanthins correspond to blue light and are between 320 and 475 nm. The emission maxima correspond to green light, and measured wavelengths are between 506 and 660 nm.26−29 Although it was thought that betacyanins do not fluoresce,28 findings of Sandquist and McHale30 proved that purified B


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Journal of Agricultural and Food Chemistry Table 2. Spectral and Structural Characteristics of Betanin Group Pigments7,13,38,44,47−57

C


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Journal of Agricultural and Food Chemistry Table 2. continued

D


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Table 3. Spectral and Structural Characteristics of Gomphrenin Group Pigments58−60

of cyclo-DOPA, whereas betaxanthins exhibit an absorbance maximum at 471.5 ± 13.5 nm.25 Spectrophotometry is the most straightforward method to quantify betalains. In 1970, Nilsson33 established a spectro-

photometric approach to quantify batalainic pigments from fresh red beets, on which future studies relied, even when studying thermal degradation kinetics.11 However, color contents can be overestimated.34 Advanced analytical instruE


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Journal of Agricultural and Food Chemistry Table 4. Spectral and Structural Characteristics of Amaranthin Group Pigments42,60−62

the bougainvillein group (Table 5) associates carboxylated as well as decarboxylated betanins referred to as 2-descarboxybetanin-type betacyanin by Strack.35 2.3. Betaxanthins. In betaxanthins, the cyclo-DOPA unit of betacyanins is replaced by an amine or an amino acid. Indicaxanthin from cactus pear was the first yellow pigment structurally characterized, having a proline moiety.8 The most commonly studied betaxanthins are indicaxanthin, the main pigment in yellow Opuntia species, and vulgaxanthin I (glutamine as substituent), the abundant betaxantin in Beta vulgaris. Residues of betaxanthins include glutamine, methionine sulfoxide, tyramine, DOPA, and 5-hydroxynorvaline. The maximum absorption of betaxanthins varies from 460 to 480 nm and is tightly linked to the structure of the amino compound. Hypso- and bathochromic shifts are then produced.67 The highest absorption maximum was displayed by indicaxanthin and portulacaxanthin I (proline and hydroxyproline residues). Noteworthy, amine conjugates display a lower absorption maximum than their respective amino acids.67−69 Under physiological conditions, betaxanthins are accompanied by free betalamic acid, exhibiting a maximum absorbance of 424 nm.51,70 Interestingly, the yellow betaxanthins were shown to be less stable than their red counterparts.11,71 Although thermal exposure induces the isomerization of indicaxanthins in cactus pear juices, de novo formation of this main compound was observed thereafter by spontaneous condensation of the released betalamic acid and the free amino compounds in the matrix juice.19 The substitution patterns and the particular sources of 36 currently identified betaxanthins are reported in Table 6.

ments including HPLC, LC−high resolution MS (LC-HRMS), LC-NMR, and 1D and 2D 13C NMR spectroscopy experiments are increasingly employed for structure determination of betalains.13,35−40 2.2. Betacyanins. The aglycon betanidin (1) is the backbone of all betacyanins. Glycosylation and acylation of the resulting 5-O- or 6-O-glucosides generate a great variety of betacyanin structures. Betanin (betanidin 5-O-ß-glucoside) (2) from red beet was the most studied pigment. Betacyanins are optically active because of their two chiral carbons (C-2 and C15). Alkaline and acid hydrolysis of betanin yielded 4methylpyridine-2, 6-dicarboxylic acid and 2,3-dihydro-5, 6dihydroindole-2-carboxylic acid.41 Glucose, glucuronic acid, and apiose are the typical sugar monomers, while sophorose and rhamnose are less frequent. Acylation of betacyanins may occur through the bond of the acyl group to the sugar moiety via an ester linkage. Malonic acid, 3-hydroxy-3-methyl-glutaric acid, caffeic acid, ρ-coumaric acid, and ferulic acid are the typical substituents. The substitution pattern of the betanidin backbone defines the absorption maximum of betacyanins. In that way, it was reported that C5 glycosylation results in a hypochromic shift and an absorbance maximum greater than that observed when C6 is glycosylated.42 Moreover, acylation with aromatic acids is more effective than esterification with aliphatic acyl moieties on the maximum absorbance of these pigments.43,44 These findings were explained by copigmentation-like intramolecular association, and a rigid conformation resulting from C6 attachment of acyl glucosides.45,46 Betacyanins can be divided into four structural types: betanin, gomphrenin, amaranthin, and bougainvillein. These structural types differ by the attachment of glucosyl groups to the oxygen atoms in the ortho position on the cyclo-DOPA moiety. The betanin-type group (Table 2) has a hydroxyl group linked to the C6 carbon and a glucosyl group on the C5 one, contrary to the gomphrenin-type group (Table 3), whose molecules are known as structural isomers of betanins. Gomphrenins are characterized by a hydroxyl group attached to the C5 carbon and a glucosyl linked to the C6 carbon. Amaranthins (Table 4) differ from the betanin structure by two contiguous glucosyl groups attached to the C5 carbon. Finally,

3. ANTIOXIDANT CHEMISTRY 3.1. Antioxidant Activity. Several studies strongly confirmed the high radical scavenging activity of betalains,88−92 which are considered as a class of dietary cationized antioxidants.93 Many authors reported that the antiradical activity of betalains is much higher than that of Trolox (6hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid), a water-soluble derivate of vitamin E,24,94 ascorbic acid,83,95 F


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Journal of Agricultural and Food Chemistry Table 5. Spectral and Structural Characteristics of Bougainvillein Group Pigments38,39,46,63−66

G


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rutin,95 catechin,93,95 ß-carotene,96 and α-tocopherol.90,93 Betalamic acid, the core structure of betalain pigments, was shown to reduce 2 molecules of Fe3+ to Fe2+ and therefore is able to donate 2 electrons to an oxidizing agent.97 Furthermore, betalamic acid exhibits a pKa of 6.8. Consequently, a pH dependence of betalains’ antiradical activity was reported.97 While betanin exhibits a high radical scavenging activity at pH > 4, the highest activity of betanidin was reported at pH values between 2 and 4. In basic pH, mono-, di-, and tri-deprotonated forms of betanin were detected, whereas the cationic form of betanidin was reported at acidic pH.98 In the case of betaxanthins, the presence of a catechol substructure results in an elevated antioxidant activity at higher pH.24 The reduction potential of betanin and indicaxanthin was evaluated respectively at 0.4 and 0.6 V, indicating that these two pigments are able to donate easily their electrons. At very low concentrations, betanin was demonstrated to inhibit lipid peroxidation and heme decomposition.93,95,99−101 The antioxidant activity of betalain molecules varies according to their chemical structures (Table 7). Betanidin was the most potent antioxidant against peroxyl radicals and nitric oxide.99 Dopaxanthin exhibited higher antiradical activity than isobetanin and betanin. This latter showed an enhanced activity compared to betanidin in both aqueous and lipid bilayers.90,93 Similarly, simple gomphrenin pigments showed an increased antiradical scavenging activity, compared with acylated gomphrenins, betanin, amaranthin, and dopaxanthin counterparts.83,93 Moreover, indicaxanthin was shown to be less effective than betanin in radical scavenging reactions.100 Betanin was also shown to act as an oxidation retarder, and additive effects with α-tocopherol were reported for both betanin and indicaxanthin.90,91 Once oxidized, betalains may be broken down, leading to the liberation of betalamic acid. Betalamic acid may condense thereafter with cyclo-DOPA or amino acids to form de novo betalains. Dopachrome and cyclo-DOPA 5-O-D-glucoside radicals were reported as oxidation products of betanin, whereas betanidin oxidation with peroxyl radicals yielded betanidin quinone.90 A recent study reported that the nonenzymatic oxidation of betanin and 2-decarboxybetanin

results primarily in the formation of 2-decarboxy-2,3dehydrobetanin and 2-decarboxyneobetanin, respectively. This reaction yields the 2-decarboxybetanin quinone methide and produces the stable intermediate, 2-decarboxy-2,3-dehydrobetanin.102 The main oxidation compound for both 17decarboxybetanin and 2,17-bidecarboxybetanin is 2,17-decarboxy-2,3-dehydrobetanin. This product is obtained after the irreversible decarboxylation of the 17-decarboxybetanin quinone methide or by the oxidation of 2,17-bidecarboxybetanin.102 Regarding the oxidation of neobetanin, a decarboxylative transformation of the formed neobetanin quinone methide yields the 2-decarboxy-2,3-dehydroneobetanin.102 Some of betacyanin’s oxidation products are shown in Figure 2. Further studies are required to identify the oxidation residues of the most important pigments. Moreover, the role of betalain pigments in oxidoreductive reactions and their interaction type with standard antioxidants should be assessed. 3.2. Structure−Activity Relationship. Structurally, betalains are immonium derivatives of betalamic acid that contain an aromatic amino compound which is able to stabilize radicals. This stabilization is tightly linked to betalain’s electron donation ability. As radicals are electron deficient molecules, betalains are able to donate electron density to the half-filled orbital, and ensure their stabilization.89 A radical’s stability can be determined using the bond dissociation energies (BDE) of the C−H bonds that must be homolytically cleaved in order to obtain the radicals. Low BDE reflects the formation of stable free carbocations, and high BDE reflects the formation of unstable ones. As illustrated in Figure 3, BDE decreases from methyl to allylic and benzylic.103 Hence, betalains remain stable after their reaction with free radicals. Moreover, free radicals are stabilized by resonance: The π system of the double bond interacts with the σ bonds of the substituents rendering the alkyl groups on a CC double bond as electron donors for the π system. This resonance phenomenon is called hyperconjugation.104,105 The antioxidant activity of betalain molecules depends on their chemical structure. A recent study24 reported that the calculated Trolox equivalent antiradical capacity (TEAC) value of betalains without aromatic resonance, charge, or hydroxy H


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Journal of Agricultural and Food Chemistry Table 6. Spectral and Structural Characteristics of Betaxanthin Pigments17,48,60,61,64,67,72−87

groups is 2.4 ± 0.1 units. This value is about 1.8 ± 0.1 units for betalains with charge and no aromatic resonance, and increases to 2.8 ± 0.4 units for compounds carrying an aromatic ring. The TEAC value reaches 4.1 ± 0.3 units for betalains having a six-membered benzene ring fused to a five-membered nitrogencontaining ring, forming an indoline group. The presence of a charged imino group ion seems to decrease the antiradical activity. Interestingly, no effect related to the carboxylation of these pigments was noted.24 In betaxanthins, the antioxidant

activity is a function of the number of hydroxy and imino residues. In betacyanins, it was demonstrated that acylation raises the antioxidant potential, whereas glycosylation decreases these pigments’ activity. Furthermore, 6-O-glycosylated betacyanins exhibit higher free radical scavenging activity than 5-Oglycosylated counterparts.10 3.2.1. Stabilization by the Phenolic Hydroxy Groups. In phenolic hydroxy groups, the alcohol functional group consists of an O atom bonded to an sp2-hybridized aromatic C atom I


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Journal of Agricultural and Food Chemistry

bond distance, (2) a more basic hydroxyl oxygen, and (3) a more acidic hydroxyl proton (−OH).106,107 The polar nature of the O−H bond of the phenol group (due to the electronegativity difference of the atoms) results in the formation of hydrogen bonds with other phenol molecules or other H-bonding systems, and implies a high solubility in aqueous media. A recent study89 revealed that the calculated BDE of C6−OH of different mono-, di-, and tri-deprotonated forms of betanin decreases with the increasing level of betanin molecule deprotonation. The authors deduced that betanin is a good hydrogen and electron donor, with elevated free radical scavenging activity. At higher pH, where betanin occurs in tri-deprotonated form, the BDE C6−OH reaches a value nearly 60 kcal/mol. As intrinsically electron rich compounds, phenols are prone to enter into efficient electron-donation reactions with oxidizing agents. An electron is transferred from a phenol to the unfilled orbital of one-electron oxidant, producing a phenoxyl radical PhO• (or phenolate radical) (eq 1).

Table 7. Antioxidant Activities of Some Studied Betalains EC50 (μM) compound betacyanins betanin isobetanin amaranthin betanidin isoamaranthin iresinin celosianins gomphrenin I gomphrenin II gomphrenin III betaxanthins dopaxanthin 3-methoxytyraminebetaxanthin (S)-trypthophanbetaxanthin standard antioxidants ascorbic acid rutin (+)-catechin ferulic acid α-tocopherol

DPPH 4.88 4.89 8.37

linoleic acid

inhibition (%)

0.4

50.08 50.08 31.1

refs

8.35 8.08 7.13 3.35 4.11 4.11

31.1 32.4 34.6 74.5 59.9 59.9

83, 93 83 83 93 83 83 83 83 83 83

4.08 4.21

60.03 56.9

83 83

53.6

83

0.8

Ph − OH + R· → Ph − O· + RH 13.93 6.11 7.24 19.35

1.2 5

17.1 40.9 33.7 14.7

(1)

The result is the transfer of a hydrogen atom from the phenolic hydroxyl group to the free radical. The phenoxyl radical is stabilized by resonance delocalization of the unpaired electron to the ortho and para positions of the ring, as shown in Figure 4.

83 95 93, 95 95 93

Figure 4. Resonance stability in phenoxyl anion.

The stability of the phenoxyl radical is increased by hydrogen bonding, such as an adjacent hydroxyl or amino group (Figure 5). This may explain both the enhanced stability and antiradical

Figure 5. Hydrogen bonding stabilization.

Figure 2. Some of betacyanin’s oxidation products: (a) 2-decarboxy2,3-dehydrobetanin, (b) betanidin quinone, (c) dopachrome, (d) cycloDOPA 5-O-D-glucoside radical.

activity of betalains containing more than one phenolic hydroxy ́ group, compared to their counterparts. Gandia-Herrero et al. reported that the presence of two phenolic hydroxyl groups in the pigment implies an increase of the TEAC value by 3.4 units.94 Indeed, it is important to note that the −OH groups linked to the sugar moieties of betacyanins are not H-donors and consequently do not exhibit any antioxidant activity.95 The radical chain reaction is stopped when the phenoxyl radical reacts with a second one electron oxidant molecule, leading to the formation of a peroxycyclohexadienone (eq 2). 3.2.2. Stabilization by the Imino and the Tetrahydropyridine Groups. In addition to alkyl groups, free radicals are stabilized by adjacent groups with lone pairs, such as oxygen and nitrogen. The nitrogen in an amine is electronegative and able to donate its loan pair into a p system. Therefore, it has

Figure 3. Radicals’ stability.

and a H atom via s bonds. The polarity of the C−O and the O−H bonds is ascribed to the high electronegativity of the oxygen. Conjugation exists between an unshared electron pair on the oxygen and the aromatic ring. Compared to simple alcohols, this structure results in (1) a shorter carbon−oxygen J


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processing and storage by choosing appropriate temperature and pH, and minimizing oxygen and light access.12,119 Temperature is an important factor since betalains are known as heat sensitive molecules. Their degrading rate depends on the temperature level and the heating period.120 In general, within the optimal area of pH stability, thermal degradation of these pigments is associated with color loss or browning, due to the subsequent polymerization. Several studies reported that betalains remain stable when processing and/or storage temperatures are below 50 and 60 °C, 60 and 75 °C,121 and 70 and 80 °C.120 Reshmi et al. reported that betacyanins from Basella alba are stable between 0 and 20 °C.122 During heat processing, betanin may be degraded by isomerization, decarboxylation, cleavage or dehydrogenation. Although dehydrogenation leads to the formation of neobetanin, thermal cleavage results in the release of betalamic acid and the colorless cyclo-DOPA-5-O-glycoside, in an unstable form.123,124 Regarding pH, betalains are stable over a broad pH ranging from 3 to 7. They can degrade below pH 2 and above pH 9.10,73 At pH greater than 8, hypochromic shifts are observed, indicating the release of betalamic acid. Therefore, the absorption at 400−460 nm increases whereas its intensity decreases at 540−550 nm.122 Alkaline pH induces aldimine bond hydrolysis, whereas low pH values are associated with C15 isomerization of betanin and betanidin into isobetanin and isobetanidin.10,125,126 Recondensation of betalamic acid and the amino compound (betaxanthins) or cyclo-DOPA-5-O-ß-glucoside was also reported under acidic conditions.11 However, betalain degradation mechanism remains unclear. Under elevated temperatures, the optimum pH that ensures betanin’s stability is toward 6. In the presence of oxygen, betanin is stable at pH between 5.5 and 5.8. Anaerobic conditions require lower pH values ranging from 4.0 to 5.0. Although they are stable between pH values ranging from 4 to 7, the greatest betaxanthin stability was evaluated at pH 5.5, which corresponds to the optimum pH of betacyanins.11,127 Finally, it is recommended to allow freshly processed extracts to stand for pH values about 5 and temperatures below 10 to allow betacyanin regeneration from early degradation products.123,128 Besides antioxidants, metal chelating agent EDTA, and inclusion complexes using maltodextrin and ß-cyclodextrin, encapsulation is an efficient method allowing stabilization and ease of betalains’ administration. Encapsulation has been investigated in polyphenol stabilization and improvement of their bioavailability.129,130 With respect to betalains, encapsulation using polysaccharides such as pectin or guar gum as wall materials allowed reducing their hygroscopicity and enhancing their stability.131 Encapsulation of Amaranthus betacyanins using maltodextrin (MDE, 10−25 dextrose equivalent DE) as carrier and starch as coating agent allowed enhancement of pigment stability and reduction of color loss during a four-

both −I and +R effects. However, the +R effect is greater than the −I effect. These electronic effects greatly influence the reactivity of the free radicals. In fact, thanks to its lone pair of electrons, the nitrogen can stabilize the radical through resonance (+R). It is also very nucleophilic, consequently it will not react with electron rich alkenes.108−110 The radical quenching activity of betalain pigments is basically supported by the “intrinsic activity” shared between the imino and the tetrahydropyridine groups.94 The common electronic resonance system supported between the two nitrogen atoms allows creating a stable carbocation upon an electron abstraction (Figure 6). This may explain the reducing properties of betalamic acid.97 Regarding the tetrahydropyridine group, the BDE for H− N16 is nicely consistent with pH increased TEAC values of some studied forms of betanin. At this level, a higher degree of betanin deprotonation implies a lower BDE value, and therefore betanin donates more easily its hydrogen atom.89 The stabilization of free radicals by the nitrogen atom explains the antioxidant properties of betalains without aromatic resonance, charge, or hydroxy groups,24 and those of betaxanthins derived from proline,100 tryptophan,95 and glutamic acid.111 Finally, the radical scavenging activity of the tetrahydropyridine group may be associated with its common electronic resonance,94 as shown in Figure 6. Tetrahydropyridine stabilization by hydrogen bonding with the adjacent carboxylic groups is also probable (Figure 7). Further investigations are required to provide more detailed mechanistic aspects of the structural implications of betalain pigments in oxidoreductive reactions.

4. FACTORS AFFECTING BETALAINS’ STABILITY During processing and storage, many factors can alter the stability of betalain pigments and lead to the loss of their color and functional properties. These factors involve temperature, pH water activity, light, and the presence of metal cations.11 Endogenous enzyme activities such as ß-glucosidases,112,113 polyphenoloxidases,114,115 and peroxidases112,116 contribute to pigment discoloration. Interestingly, betacyanins are more prone to peroxidase activity than betaxanthins, which are completely suppressed upon catalase addition.117 In red beet, betalain oxidation was reported to release cyclo-DOPA-5-O-ßglucoside, betalamic acid, and 2-hydroxy-2-hydrobetalamic acid.118 Enzymatic degradation can be handled during

Figure 6. Radical stabilization by the common resonance system shared between the imino and the tetrahydropyridine groups. K


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Figure 7. Stabilization by hydrogen bonding in the tetrahydropyridine group.

month storage period.132 Similarly, it was reported that encapsulation with MDE (10 DE) of Opuntia lasiacantha Pfeif fer betanin extract led to a reduction on pigment loss up to 14% after 6 months of storage in dark at 25 °C.133 These results ́ were corroborated by those of Gandia-Herrero and co134 workers, who reported that stability of miraxanthin V and betanidin, assessed using HPLC, was highly promoted by encapsulation using chitosan and maltodextrin, with limited pigment loss after six months storage and retained antioxidant activities. Regarding betaxanthins, it was reported that encapsulating purified indicaxanthin with MDE (20%, w/v) results in pigment stabilization without affecting the color intensity and prevention of pigment degradation during storage in the dark at 4 and 20 °C for more than six months.135 Interestingly, it was shown that encapsulated indicaxanthin extract is more stable than that of betacyanin at 60 °C.136 Different betalains’ stabilization methods were recently reviewed.137

(3) Brockington, S. F.; Yang, Y.; Gandia-Herrero, F.; Covshoff, S.; Hibberd, J. M.; Sage, R. F.; Wong, G. K.; Moore, M. J.; Smith, S. A. Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales. New Phytol. 2015, 207, 1170−1180. (4) Gill, M. Pigments of fungi (Macromycetes). Nat. Prod. Rep. 1994, 11, 67−90. (5) Steglich, W.; Strack, D. Betalains. In The Alkaloids, Chemistry and Pharmacology; Brossi, A., Cordell, G. A., Eds.; Academic Press Inc.: San Diego, CA, 1992; Vol. 42, pp 1−62. (6) Mabry, T. J.; Dreiding, A. S. The betalains. In Recent advances in phytochemistry; Mabry, T. J., Alston, R. E., Runeckles, V. C., Eds.; Appleton: New York, 1968; pp 145−160. (7) Wyler, H.; Mabry, T. J.; Dreiding, A. S. Zur Struktur des Betanidins-Ü ber die konstitution des Randenfarbstoffes Betanin. Helv. Chim. Acta 1963, 46, 1745−1748. (8) Piattelli, M.; Minale, L.; Prota, G. Isolation, structure, and absolute configuration of indicaxanthin. Tetrahedron 1964, 20, 2325− 2329. (9) Esatbeyoglu, T.; Wagner, A. E.; Schini-Kerth, V. B.; Rimbach, G. BetaninA food colorant with biological activity. Mol. Nutr. Food Res. 2015, 59, 36−47. (10) Stintzing, F. C.; Carle, R. Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci. Technol. 2004, 15, 19−38. (11) Herbach, K. M.; Stintzing, F. C.; Carle, R. Betalain stability and degradation-structural and chromatic aspects. J. Food Sci. 2006, 71, R41−R50. (12) Delgado-Vargas, F.; Jiménez, A. R.; Paredes-López, O. Natural pigments: carotenoids, anthocyanins and betalains. Characteristics, biosynthesis, processing and stability. Crit. Rev. Food Sci. Nutr. 2000, 40, 173−289. (13) Strack, D.; Vogt, T.; Schliemann, W. Recent advances in betalain research. Phytochemistry 2003, 62, 247−269. (14) Schliemann, W.; Kobayashi, N.; Strack, D. The decisive step in betaxanthin biosynthesis is a spontaneous reaction. Plant Physiol. 1999, 119, 1217−1232. (15) Khan, M. I.; Giridhar, P. Enhanced chemical stability, chromatic properties and regeneration of betalains in Rivina humilis L. berry juice. LWT Food Sci. Technol. 2014, 58, 649−657. (16) Gandía-Herrero, F.; Escribano, J.; García-Carmona, F. Characterization of the activity of tyrosinase on betanidin. J. Agric. Food Chem. 2007, 55, 1546−1551. (17) Gandía-Herrero, F.; Escribano, J.; García-Carmona, F. Betaxanthins as substrates for tyrosinase. An approach to the role of tyrosinase in the biosynthetic pathway of betalains. Plant Physiol. 2005, 138, 421−432. (18) Attoe, E. L.; von Elbe, J. H. degradation kinetics of betanine in solutions as influenced by oxygen. J. Agric. Food Chem. 1982, 30, 708− 712. (19) Herbach, K. M.; Rohe, M.; Stintzing, F. C.; Carle, R. Structural and chromatic stability of purple pitaya (Hylocereus polyrhizus [Weber] Britton & Rose) betacyanins as affected by the juice matrix and selected additives. Food Res. Int. 2006, 39, 667−677. (20) Pash, J. H.; von Elbe, J. H. Betanine stability in buffered solutions containing organic acids, metal cations, antioxidants or sequestrants. J. Food Sci. 1979, 44, 72−75. (21) Czapski, J. Heat stability of betacyanins in red beet juice in betanine solutions. Z. Lebensm.-Unters. Forsch. 1990, 191, 275−278.

5. CONCLUSIONS Functional foods have gained an increased cultural and scientific interest owing to their health promoting and wellbeing properties. Betalainic foods have been investigated as natural food colorants, strong antioxidants, and sources of bioactive compounds. In 2009, betalains from red beet were able to fulfill 10% of the global demand of food colorants.138,139 Alternative food colorant sources may be commercially investigated such as cactus pears, and may not only enlarge the color spectrum offered by red beet but also contribute to the sustainability of semiarid and arid areas. Development of crops with increased betalain levels should be further investigated. The excellent water solubility of betalains could propel their use as food supplements when water solubility is crucial. However, since betalains are prone to thermal degradation, future research should focus on both interaction with antioxidants and suitable technologies to ensure the stability of these pigments during processing. Although about 78 pigments were identified, bioavailability trials should propose the most interesting ones for industrial use.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel: +21622860665. ORCID

Imen Belhadj Slimen: 0000-0002-9492-7899 Notes

The authors declare no competing financial interest.

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REFERENCES

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Chemical and Antioxidant Properties of Betalains - American

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