Physicochemical Characteristics of Starches ... - Wiley Online Library

Starch/Stärke 61 (2009) 291–299

DOI 10.1002/star.200800103

Vicente Espinosa-Solisa Jay-lin Janeb Luis A. Bello-Pereza

Physicochemical Characteristics of Starches from Unripe Fruits of Mango and Banana

a

Mango and banana starches were isolated from unripe fruits and their morphology; thermal and pasting properties; molar mass and chain length distribution were determined. Mango starch granules were spherical or dome-shaped and split, while banana starch had elongated granules with a lenticular shape. Amylopectin of both fruit starches had a lower molar mass than maize starch amylopectin; however, mango amylopectin had the highest gyration radius. Banana amylopectin showed the lowest percentage of short chains [degree of polymerization (DP) 6–12] and the highest level of long chains (DP 37); mango amylopectin presented the highest fraction of short chains, but the level of longest chains was intermediate between those of banana and maize amylopectins. Banana starch presented the highest average gelatinization temperature followed by mango starch and maize starch had the lowest value; a similar pattern was found for the gelatinization enthalpy. The two fruit starches had a lower pasting temperature than maize starch, but the former samples showed higher peak and final viscosities than maize starch. Structural differences identified in the fruit starches explain their physicochemical characteristics such as thermal and pasting behavior.

Centro de Desarrollo de Productos Bióticos del IPN, Yautepec, Morelos, México b Department of Food Science and Human Nutrition, Iowa State University, Ames, IA, USA

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1 Introduction Most of the structural and physicochemical characterizations of starch have been performed in wheat, maize, potato and rice starches because of their commercial importance. In contrast, little is known about structural and molecular characteristics of starch from unconventional sources, such as green banana and mango fruits. However, diverse studies, where their physicochemical and functional properties were tested, have demonstrated potential application [1–7]. Banana (Musa paradisiaca L.) and mango (Mangifera indica L.) are climacteric fruits. In México and many other countries they are consumed in the ripe state. For this reason, large quantities of fruits are lost during shipping resulting from an improper postharvest handling. The large starch contents of these fruits at unripened state (70–80%) make the fruits a potential source of starch for various applications [1].

they reported the physicochemical and morphological properties. Recently, the structural characteristics and in vitro digestibility of mango kernel starch from the varieties chausa and kuppi were reported [9]. Limited studies on starch structural characteristics of banana variety “macho” [10] and mango “Tommy Atkins” variety were reported [10]. However, the fine structure of amylopectin of these starches has not been studied in detail. This information is important to relate the structures to physicochemical and functional characteristics such as pasting behavior, gelatinization and retrogradation phenomena. The present work analyzed the structural and physicochemical properties of two starches from unconventional sources: banana variety “macho” and mango variety “Tommy Atkins”, using scanning electron microscopy (SEM), iodine titration, high-performance size-exclusion chromatography equipped with multi-angle light-laser scattering and refractive index detectors (HPSEC-MALLS-RI), fluorophore-assisted capillary electrophoresis (FACE), differential scanning calorimetry (DSC) and pasting properties.

Banana and mango starches have not been extensively studied but there have been investigations of different varieties of these fruits. Kuar et al. [8] studied starch isolated from mango kernels (seeds) from five varieties and

2 Materials and Methods

Correspondence: Luis A. Bello-Perez, Centro de Desarrollo de Productos Bióticos del IPN, Apartado postal 24 C.P., 62731, Yautepec, Morelos, México. Phone: 152-735-3942020, Fax: 152735-3941896, e-mail: [email protected].

Unripened bananas (Musa paradisiaca L.) from the variety “macho” were purchased in the local market in Cuautla (Mexico) immediately after harvesting without any postharvest treatment. The skin color and size were the pa-

© 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

2.1 Starch isolation

www.starch-journal.com

Research Paper

Keywords: Mango; Banana; Structure; Amylopectin

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rameters used for cutting of the fruit. Unripened mangos (Mangifera indica L.) from the cv. “Tommy Atkins” were also purchased in the local market. Both starches were isolated using a pilot-scale procedure proposed by Kim et al. [11]. The fruits were peeled, cut into 5–6 cm cubes (100 kg total weight), immediately submerged in aqueous citric acid solution (0.5 g/L) and then macerated at low speed in a Waring blender (10 kg of fruit to 10 L of solution) for 2 min. The homogenate was consecutively sieved through screens (20, 40, 100 and 200 US mesh) until the wash water (distilled) was clear, and then it was centrifuged in a semicontinuous centrifuge (Veronesi model BSGAR 1500, Verona, Italy) at 10,7506g. The sediments from the 100 and 200 US mesh screens were washed and then centrifuged. The processes of sieving and centrifuging for starch isolation and purification were repeated three times. The starch sediments were dried in a spray dryer (Niro Atomizer model P-6.3. Copenhagen, Denmark), with a feeding temperature of 130–1507C, a solids concentration in the feeding line of 300–400 g/kg and an air outlet temperature of 70–807C. The powder was ground to pass a US No 100 sieve and stored at room temperature (257C) in a glass container. Normal maize starch was obtained from Arancia, productos de maíz (Toluca, Estado de Mexico).

2.2 Apparent amylose content Starch samples were defatted using a Soxhlet apparatus and 85% methanol solution for 24 h. The samples were washed with ethanol and recovered by filtration. Iodine affinities of defatted starch were measured using an automatic potentiometric titrator (702 SM Tirino, Metrohm, Herisau, Switzerland) following the method previously reported [12]. Apparent amylose contents were calculated by dividing the iodine affinity of defatted starch by 20% [13].

2.3 Starch granule morphology Starch granules, spread on silver tape and mounted on a brass disk, were coated with gold/palladium (60/40). Sample images were observed at 15006magnification under a scanning electron microscope (JOEL, model JSM-5800LV, Tokyo, Japan) at Bessey Microscopy Facility, Iowa State University.

2.4 Molar mass and gyration radius of amylopectin Weight-average molar mass and z-average gyration radius of amylopectin were determined using HPSECMALLS-RI. Starch samples were prepared as described by Yoo and Jane [14]. The HPSEC system consisted of a


Starch/Stärke 61 (2009) 291–299 HP 1050 series isocratic pump (Hewlett Packard, Valley Forge, PA, USA), a multi-angle laser-light scattering detector (Dawn DSP-F, Wyatt Tech. Co., Santa Barbara, CA, USA) and a HP 1047A refractive index detector (Hewlett Packard, Valley Forge, PA, USA). To separate amylopectin from amylose, a Shodex OH pak KB-guard column and KB-806 and KB-804 analytical columns (Showa Denko K.K., JM Science, Grand Island, NY, USA) were used. Operating conditions and data analysis were the same as described by Yoo and Jane [15], except that the flow rate used was 0.5 mL/min and sample concentration was 0.3 mg/mL.

2.5 Amylopectin branch chain-length distribution Starch was fractionated using GPC, following the method of Song and Jane [16]. The amylopectin fractions were collected, evaporated, and precipitated with ethanol. Isolated amylopectin was analyzed for chain-length distribution using FACE as essentially described by [17, 18]. Amylopectin was dispersed in 90% dimethyl sulfoxide (DMSO) solution, precipitated by ethanol, and centrifuged at 67506g for 15 min. Amylopectin was suspended in water to give 2 mg amylopectin per milliliter water. The mixture was heated in a boiling water bath for 30 min and then cooled down to room temperature. Eighty microliters of the mixture was added with 19 mL acetate buffer solution (50 mM, pH 3.5) containing 0.02% sodium azide, and digested with 1 unit isoamylase from Pseudomonas sp. (Megazyme International, Wicklow, Ireland) at 407C for 2 h. The digested sample was heated in a boiling water bath for 10 min to inactivate the isoamylase. Fifty microliters of the sample were evaporated to dryness in a centrifugal vacuum evaporator. The reductive amination reaction of the reducing end was performed by adding 2 mL of 0.2 M aqueous 8-amino1,3,6-pyrenetrisulfonic acid (APTS: Sigma. Aldrich Co., St. Louis, MO, USA) and 2 mL of 1 M aqueous sodium cyanoborohydride to the dry sample. The mixture was incubated at 407C for 18 h, and then 46 mL of deionized water were added. An aliquot of 10 mL was diluted to 200 mL with deionized water. Analysis of chain-length distribution of amylopectin was conduced using a Beckman P/ACE capillary electrophoresis instrument with the 50 cm length N-CHO coated capillary (50 cm diameter) and a separation Gel Buffer-N (ProteomeLab™ Carbohydrate labeling and analysis kit: Beckman Coulter, Inc., CA, USA) sample was introduced by pressure injection 5 s at 3447 Pa (0.5 psi).

2.6 Thermal properties of starch Thermal properties of starch were determined using a differential scanning calorimeter (DSC-7, Perkin-Elmer, www.starch-journal.com

Starch/Stärke 61 (2009) 291–299

Characteristics of Starches from Unripe Fruits of Mango and Banana

Norwalk, CT, USA) [19]. Starch (2 mg, dsb) was accurately weighed in an aluminum pan, mixed with 6 mg of deionized water and sealed. The sample was allowed to equilibrate for 1 h and scanned at a rate of 107C/min over a temperature range of 10–1107C. An empty pan was used as the reference. The rate of starch retrogradation was determined using the same gelatinized samples, stored at 47C for seven days, and analyzed using the same process described for gelatinization. All thermal analyses were conducted in triplicate for each sample.

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banana starch was in agreement with that reported for banana starch isolated from the same variety (37%) [23] and from another variety (40%) [24], using the same method. The amylose content of the mango fruit starch was similar to that used for resistant starch preparation from the same variety “Tommy Atkins” (28.7%) [7]. However, two other varieties, “criollo” (12.9%) and “manila” (13.3%) presented lower apparent amylose content [6].

3.2 Starch granule morphology 2.7 Pasting properties of starch Starch pasting properties were analyzed using a Rapid Visco Analyser (RVA-4, Foss North America, Eden Prairie, MN, USA) [19]. A starch suspension (8%, w/w, dsb), in triplicate for each sample, was prepared by weighing starch (2.24 g, dsb) into a RVA canister and making up the total weight to 28 g with deionized water. The starch suspension was equilibrated at 307C for 1 min, heated at a rate of 6.07C/min to 957C, maintained at 957C for 5.5 min, and then cooled to 507C at a rate of 6.07C/min. Constant paddle rotating speed (160 rpm) was used throughout the entire analysis.

Scanning electron micrographs of normal maize (A), mango fruit (B) and banana (C) starch granules are shown in Fig. 1. Mango starch granules were spherical or domeshaped and split. Mango starch granules present some indentations that could be due to non-uniform growth within starch granule or collapse during drying. This kind

3 Results and Discussion 3.1 Apparent amylose content Iodine affinities and corresponding apparent amylose contents of normal maize, mango fruit and banana starches are shown in Tab. 1. Apparent amylose was different for the starches analyzed. Banana starch had the largest apparent amylose content (36.2%), followed by mango (31.1%) and normal maize starch (29.7%). The difference in amylose content affect the physicochemical and functional properties, because starches with higher amylose contents produce firmer and more opaque gels with

Tab. 1. Iodine affinities and apparent amylose content for defatted starches. Source

Iodine affinitya

Apparent amylose contentb [%]

Normal maize Mango Banana

5.93 6 0.06 6.21 6 0.19 7.24 6 0.24

29.7 31.1 36.2

a) Averaged from three replicates 6 standard deviation. b) Calculated as C= IAS/0.20 where C is the percentage of apparent amylose content and IAS is the iodine affinity of the whole defatted starch.

Fig. 1. Scanning electron micrographs of normal maize (A), mango (B) and banana (C) starches (15006) (scale bar = 20 mm).



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of morphology has been found for other fruits such as winter squash [25], apple [26] and in cassava [27]. The granule sizes of mango starch were similar to those of the small granules population of maize starch, between 5–10 mm. This range was in agreement with those of starches isolated from two mango varieties [6]. Banana starch had elongated granules, with a lenticular shape, where the average longitudinal dimension was 40 mm and the short radius around 20 mm, which is in agreement with other reports of granule size and shape of banana starches [2, 28]. The granule size of normal maize starch ranged between 10–15 mm, with a higher heterogeneity showing round, oval and polygonal shapes. Sizes and shapes of starch granules influence some physicochemical, functional and nutritional characteristics, because larger granules develop a high paste viscosity and small granules are more digestible.

3.3 Molar mass and gyration radius of amylopectin Weight-average molar mass (Mw) and gyration radius (Rz) of normal maize, mango and banana amylopectins are shown in Tab. 2. Normal maize and mango amylopectins presented similar Mw values, and these were higher than those of banana amylopectin. This pattern is in agreement with the Rz value, mango amylopectin displayed the largest gyration radius (298 nm) and banana amylopectin had the smallest (267 nm). The Mw for normal maize obtained in this study agreed with data in the literature [15]. The molar mass and gyration radius of banana amylopectin were slightly higher than that in the literature [15], which could be attributed to different varieties of banana starches. The Mw of amylopectin of the three starches decreases with increasing amylose content. A similar inverse correlation has being found in other studies [9, 10, 15]. It was reported that the molar mass has influence on the pasting viscosity of the starch [29]. Studies in amylopectin of diverse botanical origins gave Mw ranging between 5.46107 and 1.16108 g/mol and Rz between 171 and 242 nm [30]. Maize amylopectin solubilized using a

Tab. 2. Average amylopectin molecular weight and gyration radius of starches. Source

Mw6108 [g/mol]a,b

Rz [nm]a,c


5.154 6 0.065 5.013 6 0.177 3.371 6 0.179

281.10 6 1.980 297.85 6 1.202 267.10 6 5.515

a) Averaged from two replicates. b) Weight-average molar mass. c) z-average radius of gyration.


microwave heating for 35 s had Mw of 2.26108 g/mol and Rz of 229 nm [31]. Amylopectin of diverse botanical sources presented Mw between 2.96107 and 3.56108 g/mol, and Rz between 95-340 nm [32], and Mw between 1.3 and 56.86108 g/mol, and Rz between 201-782 nm [15]. Amylopectin of Tef starch isolated from diverse cultivars presented Mw 1.0 and 1.46108 g/mol, and Rz between 156 and 205 nm [29]. The studies above mentioned used a HPSEC-MALLS-RI system similar to that utilized in this work.

3.4 Amylopectin branch chain-length distribution Amylopectin branch chain-length distribution for the starches of normal maize, mango and banana are shown in Fig. 2 and summarized in Tab. 3. Normal maize has few short chains of DP 6 and content in chains of DP 7 and 8 gradually increases. This is characteristic of cereal starches. Banana starch also showed an increase in chains of DP 6-8, but it more pronounced than in case of normal maize. Mango starch displays a higher population of short chains of DP 7 than DP 6 and 8. This branch chain distribution has been found for some tubers, root, and legume starches [19]. In this study, mango and normal maize starches, both had A-type polymorphism, consisted of more short chains (DP 6–12), mango (25.7%) and normal maize (24.0%), and fewer long chain (DP 37), mango (16.6%) and normal maize (13.4%), in comparison with banana starch (Ctype) [10] that displayed a lower proportion of short chains (20.5%) and a higher proportion of long chain (18.6%). This is in agreement with the results of Jane et al. [19], who reported that A-type starches had larger proportions of short chains (DP 6–12) and smaller proportion of long chains (DP 37) than B type starches. In general, the three starch samples had the largest proportion of chains with degree of polymerization (DP) between 13–24, followed by short chains with DP between 6–12 and chains with DP higher than 37. Similar pattern was found for cereal starches, in which the amylopectin had larger proportion of short chains. Slight differences were observed in the average chain lengths, with DP 21.5, 22.3 and 23.9 for normal maize, mango and banana starch, respectively. The average chain length for banana amylopectin found was comparable with that of ginkgo amylopectin, both are C-type starches [33]. Some molecular and physicochemical characteristics, such as retrogradation tendency, temperature and enthalpy of gelatinization, crystallinity percentage, etc., are related to the proportion of short chains of amylopectin [31]. www.starch-journal.com

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Fig. 2. Amylopectin chain length distribution of normal maize (A), mango (B) and banana (C) starches, measured by fluorophore-assisted capillary electrophoresis (FACE).



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Tab. 3. Branch chain-length [CL] distribution of amylopectins. Source


Average CL

Distribution [%] DP 6-12

DP 13-24

DP 25-36

DP 37

Highest detectable DP

21.5 22.3 23.9

24.0 25.7 20.5

50.2 46.1 48.1

12.3 11.6 12.9

13.4 16.6 18.6

80 84 89

Averaged from two replicates.

3.5 Thermal properties Gelatinization characteristics of the three starches studied showed differences; normal maize starch had the lowest gelatinization temperature whereas banana starch had the highest. A similar trend was found for the enthalpy changes of the starches (Tab. 4). Gelatinization of starch is the loss of the crystalline structure of the starch granule, which mainly results from crystalline amylopectin. The highest gelatinization temperature of banana starch can be attributed to its smaller proportion of short branch chains and larger proportion of long branch chain found in the amylopectin molecule (Tab. 3). The different the branch chain-length pattern of banana amylopectin agreed with the X-ray diffraction pattern (C-type). It has been reported that the type of the X-ray diffraction pattern relates to the branch chain-length distribution of the amylopectin [34]. Starches of the A-type crystalline structure consist of more short branch chains than those of the C-type crystalline structure. Retrogradation properties (Tab. 4) showed that the crystals formed during storage of gelatinized banana starch had the largest thermal stability because they dissociated at higher temperature and with a larger enthalpy change; this result indicated that a higher degree of crystallinity was produced in banana starch than in the other starches analyzed. It is also noticed that the dissociation temperatures of the retrogradation starch samples were lower

than the gelatinization temperatures, because during the retrogradation small and/or less perfect crystals were formed [35, 36]. Mango starch displayed the least percentage of retrogradation and banana starch the highest. The lower degree of retrogradation of mango starch could be attributed to the larger proportion of short branch chain of amylopectin [37, 38] and its lower lipid content than normal maize starch. Fast retrogradation of banana starch was reported; after 14 h of storage at low moisture content some peaks of crystallinity were found and the polymorphism of the retrograded banana starch was Atype [36].

3.6 Pasting properties The pasting properties of starch are influenced by other components present in the starch suspension during heating as well as the interactions between the starch molecules in the granule [39-41]. When a starch suspension is heated at a constant rate, the viscosity increases gradually until a maximum value is reached (Fig. 3). The pasting temperatures for the starch samples were in the order: normal maize . banana . mango (Tab. 5). Banana starch showed the largest peak viscosity and normal maize the lowest. The difference between the DSC gelatinization onset temperature (T0) and the pasting temperature of a particular starch was greater for normal maize starch than for mango and banana starches. This diffe-

Tab. 4. Thermal properties of native and retrograded starch from normal maize, mango and banana. Source

Starch gelatinization

T0 [7C]* Normal maize Mango Banana

TP [7C]*

TC [7C]*

Starch retrogradation ˜H [J/g]*

63.9 6 0.2 68.7 6 0.3 73.2 6 0.4 13.4 6 0.3 66.5 6 0.2 71.3 6 0.3 76.1 6 0.3 14.0 6 0.7 70.9 6 0.6 76.5 6 0.9 83.3 6 1.0 16.5 6 0.7

T0 [7C]*

TP [7C]*

TC [7C]*

˜H [J/g]*

37.3 6 0.5 50.2 6 0.2 61.5 6 0.8 7.2 6 0.6 39.9 6 2.3 52.7 6 1.4 62.3 6 0.1 5.4 6 0.0 42.1 6 0.6 56.5 6 2.4 67.7 6 0.4 9.4 6 1.9

% Retrogradation 53.6 38.4 56.9

* = Onset temperature [T0], peak temperature [Tp], completion temperature [Tc] and enthalpy change [˜H]. Values are averages of three replicates of each sample.



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Fig. 3. Rapid Visco Analyser profiles of normal maize (o), mango (n) and banana (^) starches (8% dsb). Tab. 5. Pasting properties of starches measured by Rapid Visco Analyser.c Sourcea


Viscosity [RVU]b

Pasting temperature [7C]

84.0 6 1.5 71.3 6 0.2 79.3 6 0.3

Peak

Breakdown

Final

Setback

149.8 6 0.5 194.1 6 3.2 215.8 6 2.7

68.3 6 0.8 50.2 6 3.4 33.5 6 2.2

145.1 6 0.7 239.1 6 2.7 323.8 6 6.3

63.6 6 1.0 95.2 6 2.0 141.7 6 5.4

a) Mixture consisted of 8% (w/w, dsb) starch in water. b) Measured in Rapid Visco Analyser Units. c) Averaged from three replicates.

rence could be attributed to the restricting complexes present in normal maize starch. The peak viscosity of mango starch was obtained at a lower temperature than banana and normal maize starches, and the viscosity maintained a plateau until 957C. The maximum of the peak viscosity reflects the ability of starch granules to swell freely before their physical breakdown [42]. When starch is heated in the presence of water, the granules are swollen while some components, including amylose and small amylopectin, diffuse out, resulting in swollen and dispersed particles present in a continuous phase [43]. The starch dispersion properties were more affected by the branch chain-length distribution of amylopectin molecule than by the Mw [44]. During holding at 957C under shear the viscosity of starch pastes decreased for all

three starches, resulting from the breakdown of some swollen starch granules. Stevenson et al. [26] found a correlation between breakdown viscosity and starch structures. Their results show that starches, which display less breakdown viscosity, consist of amylopectin with more branch chains of DP 37 and less branch chains of DP (13-24) and larger apparent amylose content. The breakdown viscosity values of the three starches determined is this study were in the following order: normal maize . mango . banana, which agreed with the results of Stevenson et al. [26]. When the temperature dropped the viscosity increased, which resulted from network formation between amylose and amylopectin while retaining a certain amount of water [45, 46] and resulted in a gellike characteristic.



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4 Conclusions The investigated fruit starches had a lower molar mass than maize starch but mango starch showed the highest gyration radius. Banana starch presented the lowest amount of short chains and the highest level of long chains. Mango starch had the highest level of short chains. The average temperature and enthalpy of gelatinization were higher in the two fruit starches than in maize starch. Banana starch showed the highest retrogradation and mango the lowest. The fruit starches presented lower pasting temperature but higher peak and final viscosity than maize starch. This pattern is related to the higher amylose content of the fruit starches. The structural differences determined in the unconventional starches explain their physicochemical characteristics.

Acknowledgements We appreciate the financial support from SIP-IPN, COFAA-IPN and EDI-IPN, and the technical assistance of Dr. Sathaporn Srichuwong and Hongxin Jiang. One of the authors (VES) also acknowledges a scholarship from CONACYT-México.

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