Characterization of multi-scale structure and thermal properties of Indica rice starch with different amylose contents

Abstract

Fully understanding the relationship between multi-scale structure and thermal properties of rice starch is important for starch-based food processing. Multi-scale structures of Indica rice starch were studied from molecules to aggregation structure. Gel-permeation chromatography (GPC) and high-performance anion-exchange chromatography (HPAEC) both show that the amylopectin from debranched rice starch exhibits bimodal distributions. Compared with amylose-rich rice starch, amylopectin-rich rice starch had the highest molar- and weight-based ratio of fraction fa′ (DP 6–12) and lower molar-based ratios of fractions fb′₃ (DP ≥ 37). X-ray diffraction (XRD) and small angle X-ray scattering (SAXS) confirm that amylopectin-rich starch has the highest crystallinity and scattering intensity. Differential scanning calorimetry (DSC) results show that amylopectin-rich starch has the highest onset and peak gelatinization temperatures; however, there is no significant difference in enthalpy, which may be due to the irregular double helix. Rapid visco-analysis (RVA) shows amylose-rich starch has a higher final and setback viscosity, which may be due to amylose molecule entanglement in starch gel and higher retrogradation ability.

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1. Introduction

Rice (Oryza sativa L.) is one of the most important crops which provides staple food for more than half of the world's population, especially in Asian countries. Starch, a major carbohydrate in human diets, provides more than 50% of total caloric intake¹ and also contributes to the special characteristics of starch-based foods such as viscosity, texture, mouth-feel, and shelf-life during processing and in end products.² The processing and nutritional attributes of many foods result from the specific pasting, gelatinization and retrogradation of starch, which are definitely affected by the complex structure of starch.³

Native starch granules are widely regarded to be composed of a multi-scale structured polymer which is from nanometer to micrometer in scale, i.e. amylose and amylopectin chains (∼nm), crystalline and amorphous lamellar structure (9–10 nm), alternating amorphous and semi-crystalline growth rings (100–400 nm) and starch granules (<1–100 μm).^3–6 The two basic components in starch are near linear amylose and highly multiple-branched amylopectin, which may affect the higher level structure of starch (aggregation structure).^7–9 Although the multi-scale structure of rice starch has been widely studied, the relationship between starch molecules and aggregation structures is still not clear. Generally, it is widely regarded that the amorphous zone is amylose and the branching points are amylopectin, while the short-branched chains in the amylopectin are the main crystalline component in granular starch.¹⁰ Recently, Witt et al.⁷ have used Pearson correlation analysis to study the structural parameters of different biological origin waxy starches among molecular, crystalline and lamellar structures, the results showing that the average repeat distance decreases with increasing proportion of the shortest amylopectin branches and increases with increasing proportion of the fb′₁ (DP 13–24) and fb′₂ and fb′₃ (DP ≥ 25); however, the result is affected by the botanical origins to a large extent.

Studies of thermal properties including gelatinization and pasting properties of rice starch are very important to rice thermal processing, cooking and eating quality,¹¹ then further affecting consumer acceptability of rice. Generally, when native starch granules are heated in excess water, their semi-crystallinity is gradually eliminated, resulting in structural breakdown and starch polymer dispersion in solution.¹² Starch gelatinization reflects the crystalline structure change, and is affected by amylose and amylopectin fine structure. Jang et al.¹³ have studied the correlation between thermal properties and rice starches from Korea, the results showing that amylose content was positively correlated to pasting temperature from rapid visco-analysis (RVA), but negatively correlated to peak and breakdown viscosity. Kong et al.¹⁴ also studied the relationship between thermal properties and rice starch structure, and found that amylose content was positively correlated with peak and setback viscosity, while negative correlations were found with gelatinization temperature as measured by DSC. Amylopectin fine structure also affects starch thermal properties,¹⁵ with the fraction of short chains (DP 6–12) being negatively correlated with gelatinization temperature from DSC, and positively correlated with breakdown viscosity; in addition, fb₁ (DP 13–24) was negatively correlated with breakdown viscosity while positively correlated with setback viscosity. The effect of starch granule size on thermal properties has also been reported,¹⁶ with small and medium starch granule content being negatively correlated with gelatinization and pasting temperatures; however, large starch granule content was positively correlated with gelatinization and pasting temperatures. Although these studies have revealed the factors affecting thermal properties of rice starch, the results still did not give clear conclusions since there are few reports on how aggregation structure affects starch properties.

Fully understanding the multi-scale structure is important to design and prepare healthy starch-based foods for consumers; however, there is no comprehensive study on starch multi-scale structure from molecular to granular level. The current work aims to provide an accurate and comprehensive observation of the effect of amylose content and the fine structure of amylopectin on the higher-order structures. Hybrid varieties of Indica rice grains with different amylose content were used as model materials in this work to illustrate the relationships between different scales. The thermal properties were also studied to reveal the structure–property relationships.

2. Materials and methods

2.1. Materials

Three hybrid varieties of Indica rice grains (Xing2#, Jinnongsimiao and Yuxiangyouzhan) and one wild variety (Beihan1#) were used as model materials in this study. Detailed information can be found in Table 1. Isoamylase (from Pseudomonas sp., 1000 U mL⁻¹, EC 3.2.1.68) and pullulanase (from Klebsiella planticola, 700 U mL⁻¹, EC 3.2.1.41) used in this paper were from Megazyme, Bray, Co. Wicklow, Ireland.

Table 1 Structural parameters of rice starch from GPC

Code	Variety	Amylose content (%)	Rh,Ap1 (nm)	Rh,Ap2 (nm)	DB (%)
IR-1	Beihan 1#	6.34 ± 0.66d	1.380 ± 0.000a	2.175 ± 0.005a	7.90 ± 0.39a
IR-2	Xing2#	13.14 ± 0.22c	1.365 ± 0.005a	2.165 ± 0.005a	7.62 ± 0.72a
IR-3	Jinnongsimiao	18.45 ± 0.33b	1.335 ± 0.005b	2.130 ± 0.005b	8.30 ± 0.09a
IR-4	Yuxiangyouzhan	30.46 ± 0.50a	1.340 ± 0.010b	2.120 ± 0.010b	7.33 ± 0.05a

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2.2. Starch extraction and preparation

Starch granules were isolated from polished rice grains through wet milling and alkaline protease method with slight modifications.^17,18 Briefly, each rice grain sample (about 20 g) was steeped in 0.45% sodium metabisulfite solution overnight in a refrigerator. The grain samples were milled using a commercial food blender for 5 min, then the blended slurry was centrifuged at 2500g for 20 min before the supernatant was discarded. The residue was mixed with 0.3 mL alkaline protease to purify rice starch with the conditions of enzymatic hydrolysis, pH of 9, 45 °C for 1 h. Then the mixture was washed repeatedly with Milli-Q water and the supernatant and top yellow protein layer was discarded each time until the top layer was clear. The isolated starch was washed with ethanol, followed by drying in an oven at 40 °C for 12 h.

2.3. Gel-permeation chromatography (GPC)

Native starch granules (about 6 mg) were dissolved in DMSO/LiBr solution and debranched using isoamylase in acetate buffer (pH ∼ 3.5), following the method of Li.¹⁹ The weight distributions of debranched starch molecules were analyzed in duplicate using GPC (Agilent 1260 series, Agilent Technologies, USA) equipped with a refractive index detector (Optilab T-rEX, WYATT Corp., USA), and a differential pressure detector (Viscostar-II, WYATT Corp., USA). GPC separates molecules based on their hydrodynamic volume (V_h), or the corresponding hydrodynamic radius. The GPC weight distributions, W (log V_h), of debranched starch are denoted by W_de (log V_h); the degree of polymerization (DP) of debranched starch, amylose content and degree of branching (DB) were calculated following a method described elsewhere.²⁰

2.4. High-performance anion-exchange chromatography (HPAEC)

Amylopectin fractionation was carried out following the method of Kong.²¹ Briefly, about 3 mg fractionated amylopectin was dissolved in 150 μL 100% DMSO by constant stirring overnight to ensure full dissolution. The solution was diluted with 750 μL Milli-Q water, and 100 μL 0.1 M CH₃COONa buffer (pH 5.5); then, 1 μL isoamylase and 1 μL pullulanase were added. The debranching reaction was conducted at room temperature with slight stirring overnight and stopped by heating at 100 °C. The sample was centrifuged at 10 000g for 15 min at 4 °C and filtered (pore size 0.45 μm) before being injected into the HPAEC system.

A HPAEC system (Dionex ICS-5000+, Sunnyvale, USA) coupled with a BioLC gradient pump and a pulsed amperometric detector (PAD) was used to get the chain length distribution of debranched samples.²¹ PAD signal was recorded by Chromeleon software and corrected to carbohydrate content. Prior to loading the sample, the columns (Carbo-Pac PA-100 with a guard column) were flushed with 100 mM NaOH at a rate of 1 mL min⁻¹ for 20 min, followed by a mixture of two eluents: 100 mM NaOH (eluent A, 96%) and 100 mM NaOH containing 500 mM NaOAc (eluent B, 4%) for another 20 min. The elution gradient at a rate of 0.4 mL min⁻¹ was as follows: from 0 to 45 min, 96% eluent A; from 45 to 80 min, eluent A changed from 96 to 40% linearly; from 80 to 95 min, from 40 to 20%; from 95 to 105 min, from 20 to 96% (returned to start mixture).

2.5. X-ray diffraction (XRD)

An Xpert PRO diffractometer (PANalytical B.V., The Netherlands) was used to study the crystalline structure of starches. Samples with about 10% moisture content were equilibrated at 40 °C for 24 h before the test. All the measurements were conducted at 40 mA and 40 kV, using Cu Kα radiation with an X-ray source of 0.1542 nm wavelength. The scanning range was from 5° to 50° (diffraction angle, 2θ) with a scanning speed of 10° min⁻¹ and a scanning step of 0.033°. The crystallinity values of the samples were quantitatively estimated following our previous methods.⁹

2.6. Small-angle X-ray scattering (SAXS)

A Xeuss system (Xenocs SA, France) equipped with a multilayer focused Cu Kα X-ray source (GeniX3D Cu ULD) was used to study the lamellar structure of starch. The SAXS was conducted at 50 kV and 0.6 mA using a wavelength of 0.154 nm as X-ray radiation source. Scattering data were recorded by a semiconductor detector (Pilatus 100K, DECTRIS, Switzerland). Each SAXS pattern was collected within 30 min, background-corrected and normalized using the standard procedure.

2.7. Scanning electron microscopy

The starch powders were coated with gold in a vacuum evaporator, and then the coated specimens were viewed for their morphologies by a scanning electron microscope (JSM-7001F, Japan Electronics Corporation) at an accelerating voltage of 15 kV.

2.8. Differential scanning calorimetry (DSC)

The gelatinization behavior of starch was determined using a differential scanning calorimeter (200 F3, Netzsch, Germany) equipped with a thermal analysis data station.²² About 3 mg of starch was weighed exactly into an aluminum sample pan. Water was added to the starch in the DSC pans using a pipette to obtain a starch suspension with a water content of 75%. The pans were sealed and mixed samples were equilibrated overnight at room temperature. The pans were heated from 20 to 120 °C at a scanning rate of 10 °C min⁻¹ and an empty pan was used as the reference. All the experiments were done in triplicate. Netzsch Proteus Thermal Analysis Version 6.1.0 software was used to analyze the main endotherm of the DSC traces for onset (T_o), peak (T_p) and conclusion (T_c) temperatures and enthalpy change (ΔH).^2,23

2.9. Rapid visco-analysis (RVA)

A Newport Scientific rapid visco-analyzer 4 (RVA-4) (Newport Scientific, Warriewood, New South Wales, Australia) was used to analyze the pasting properties of starch. Starch slurries containing 8% (w/w) starch (dry weight) in a total weight of 28 g were held at 50 °C for 1 min before heating at a rate of 6 °C min⁻¹ to 95 °C, holding at 95 °C for 5 min, then cooling at a rate of 6 °C min⁻¹ to 50 °C, and held at 50 °C for 2 min.²² The speed of the mixing paddle was 960 rpm for the first 10 s and then 160 rpm for the remainder of the experiment. Some pasting-related parameters such as peak viscosity (PV), final viscosity (FV), breakdown (BD) viscosity and setback (SB) viscosity were recorded using the thermocline software.

3. Results and discussion

3.1. The molecular structure of rice starch

The GPC spectra of debranched rice starch as a function of molecular size are shown in Fig. 1. It should be noted that the isoamylase was used to get the branching structure of starch, which could catalyze α-1,6-glucosidic branch linkages in starch. From Fig. 1, it can be seen that the molecular size (R_h) distributions between 0.5 and 4 nm represent amylopectin, and small bumps at R_h > 4 nm indicate amylose.^21,24,25 Amylopectin chains show bimodal distributions, while the amylose chains show multiple small bumps. All weight R_h distributions were normalized to the same global maximum to enable relative comparison in the amylose range. From the GPC spectra, amylose content could be calculated by AUC (area under curves) of amylose/AUC of the whole starch. The shapes of amylose chain R_h distributions are different as well, indicating differences in ratios of short amylose chains to long amylose chains.

Fig. 1 GPC spectra of debranched starches as a function of molecule size.

In order to get detailed information of chain-length distributions of debranched amylopectin, HPAEC coupled with PAD was also used. Typical weight-based and molar-based chain-length profiles of debranched amylopectin are shown in Fig. 2, and four fractions were grouped according to a previous study (see Table 2).²¹ The amylopectin from all the Indica rice showed similar chain-length distribution profiles. From Fig. 2, it can be seen that there are bimodal distributions of amylopectin for all rice as expected; in detail, the first peak of weight-based bimodal chain-length profiles was at DP ∼12, while the second peak was at DP ∼44, and a shoulder at DP 18–20 was also found in all amylopectin samples, which was in agreement with a previous study.²⁶

Fig. 2 Typical chain-length distributions of amylopectin from IR-3: (A) weight- and (B) molar-based chain length distribution.

Table 2 Molar- and weight-based chain-length distributions

Code	Molar-based chain-length distribution (%)				Weight-based chain-length distribution (%)
	fa′ (DP 6–12)	fb′1 (DP 13–24)	fb′2 (DP 25–36)	fb′3 (DP ≥ 37)	fa (DP 6–12)	fb1 (DP 13–24)	fb2 (DP 25–36)	fb3 (DP ≥ 37)
IR-1	43.11	44.79	7.11	4.99	25.48	46.66	12.57	15.29
IR-2	37.26	43.34	10.00	9.40	19.02	40.42	15.79	24.77
IR-3	41.10	44.97	7.88	6.05	23.56	45.84	13.70	16.90
IR-4	29.49	54.96	12.19	3.36	17.02	54.53	20.57	7.88

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From Table 2, it can be seen that there was a relatively wide range of proportions for different groups of fractions from the debranched rice amylopectin. IR-1 with higher content of amylopectin possessed the highest molar- and weight-based ratio of fraction fa′ (DP 6–12) and lower molar-based ratios of fractions fb′₂ (DP 25–36) and fb′₃ (DP ≥ 37). IR-4 with higher content of amylose possessed the highest molar- and weight-based ratio of fraction fb′₂ (DP 13–24) and lower molar- and weight-based ratios of fractions fa′ (DP 6–12) and fb′₃ (DP ≥ 37).

3.2. Aggregation structure of rice starch

The XRD patterns of rice starches with different amylose content are shown in Fig. 3. It can be seen that all the starches exhibit A-type crystalline structure with strong reflections of 2θ at about 15, 17, 18 and 23°. It should be noticed that there is a minor peak at about 20° for those four starches, which reflects the presence of amylose–lipid complex.²⁷ The X-ray intensity of amylopectin-rich rice starch is higher than that of the amylose-rich rice starch, indicating the amylopectin-rich rice starch has higher crystallinity. The crystallinities calculated based on Fig. 3 are 29.01, 28.21, 26.02 and 24.90%. It should be noted that amylopectin-rich starch always shows a higher degree of crystallinity; however, the relationship between crystallinity and amylose content is not linear.¹⁴

Fig. 3 Typical X-ray diffractograms of rice starch with different amylose contents.

The one-dimensional (1D) SAXS scattering intensity distributions and their Lorentz-corrected profiles for rice starches are shown in Fig. 4. The scattering intensity of amylopectin-rich rice starch is higher compared with the amylose-rich rice starch, indicating a higher electron density contrast due to the differences between the crystalline lamellae and the amorphous lamellae in the starch granule.^28,29 The q peaks are 0.69, 0.68, 0.69 and 0.64 nm⁻¹, so the lamellar thickness (d = 2π/q) is about 9.10, 9.24, 9.10 and 9.81 nm⁻¹, respectively. The scattering invariant, Q , is proportional to the electron density difference between the crystalline and amorphous phases, and the volume fractions of the two phases based on a two-phase model. From Fig. 4, it is clear that the Q of amylopectin rice starch is higher compared with amylose rice starch. In a previous paper, two possible interconnected reasons, namely (a) different localization of amylose molecules within amylopectin clusters and (b) different amylopectin molecule conformation in amorphous lamellae and their packing within crystalline lamellae, are always used to explain the differences in the scattering intensity values and Q for starches with different amylose content.^30,31 Generally, waxy starch (more than 98% amylopectin) granules always show a strong lamellar peak which may be because the double helices in the semi-crystalline lamellae are oriented more uniformly.^9,32

Fig. 4 1D SAXS profiles and Lorentz-corrected 1D SAXS profiles of rice starch.

3.3. Granule structure of rice starch

Typical scanning electron micrographs of granules from rice starch with different amylose contents can be seen in Fig. 5. The granular size was observed to range from 2 to 7 μm for different rice starches. From Fig. 5, polyhedral and irregular shapes for rice starches were both seen. It has been reported that rice starches grown in tropical climates would display polyhedral, round or irregular shapes.³³ Generally, starch granules with polygonal and spherical shapes show maximum values of mean granule length. Starch granule accumulation also affects the size; for example, tightly packed granules have greater mean granular width and openly spaced granules have higher values for mean granular length.³⁴

Fig. 5 Typical scanning electron micrographs of starches from rice.

3.4. Thermal properties of rice starch

Gelatinization is important for starch-based food processing. During this processing, water will be absorbed by starch granules and cause irreversible swelling, then accompanied by amylose leaching and amylopectin solubilisation, resulting in the formation of paste. Both DSC and RVA are common tools to study the thermal properties of starch, and the results can be seen in Table 3 and 4.

Table 3 Thermal parameters of rice starch from DSC

Code	To (°C)	Tp (°C)	Tc (°C)	ΔH (J g^−1)
IR-1	63.6 ± 0.44a	70.4 ± 0.20a	75.4 ± 0.36a	11.21 ± 0.12a
IR-2	60.8 ± 0.28b	69.0 ± 0.14b	74.4 ± 0.14b	11.59 ± 0.79a
IR-3	61.1 ± 0.11b	66.3 ± 0.06c	71.6 ± 0.00c	12.29 ± 0.22a
IR-4	58.65 ± 0.07c	63.6 ± 0.21d	69.0 ± 0.14d	11.24 ± 0.30a

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Table 4 RVA pasting of rice starches

Code	Peak viscosity (cp)	Trough viscosity (cp)	Final viscosity (cp)	Breakdown (cp)	Setback (cp)
IR-1	2290 ± 12.76b	1340 ± 20.34b	1715 ± 40.23c	950 ± 10.21a	375 ± 20.36c
IR-2	2392 ± 15.56a	1505.5 ± 10.61a	2548.5 ± 45.96b	886.5 ± 4.95b	1043 ± 35.35b
IR-3	2185 ± 17.04c	1367 ± 20.62b	2570 ± 44.22b	818 ± 17.67c	1203 ± 25.57a
IR-4	1934 ± 22.02d	1532 ± 35.48a	2801 ± 50.56a	402 ± 16.62d	1269 ± 30.03a

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When starch is heated in the abound water, a large gelatinization endotherm named “G endotherm”³⁵ appearing at about 65 °C is observed from DSC (Fig. 6). From Table 3, it also can be seen that the peak and conclusion temperatures of rice starch decreased with increasing amylose content, this phenomenon being consistent with the decreased crystallinity and has been reported by Kong et al.¹⁴

Fig. 6 DSC curves of rice starch with different amylose contents.

From Table 4, it can be seen that the peak viscosity and breakdown viscosity decreased with increasing amylose content, while the final and setback viscosity increased with increasing amylose content. In fact, peak viscosity of the rice starch reflects the water-binding capacity or the extent of swelling of starch granules,³⁶ while the final viscosity may be related to the aggregation or rearrangement of the amylose molecules.³⁷ Breakdown viscosity measures the starch paste resistance to heat and shear, while setback viscosity, an index of starch retrogradation,³⁸ shows the amount of recovery of starch viscosity during cooling of the heated starch pastes, and is usually related to the amylose content of starch.

3.5. Relationship between starch multi-scale structure and thermal properties

In this study, it may be seen that the amylose-rich starch (IR-4) has the largest lamellar size, which is associated with the high fb′₁ (DP 13–24) and fb′₂ (DP 25–36), those longer chains (especially DP 13–24) are probably a reason for the increase in the production of larger crystalline lamellae. However, IR-2 with fb′₃ (longer DP ≥ 37) and less fa′ (shortest DP 6–12) may be the reason for the lower lamellar peak intensity which is due to the longest and shortest chains forming amorphous and crystalline regions, respectively.

DSC is an effective tool to observe the phase transition of starch.³⁹ When starches are heated in excess water, the “G” endotherm has been well accepted as representing the gelatinization of amylopectin. In this study, higher thermal transition temperatures of “G” peaks for amylopectin were observed; however, there is no significant difference in gelatinization enthalpy, which may be associated with a more irregular double helix structure in the crystalline structure zone in amylopectin-rich starch, which does not cause a significant difference in gelatinization enthalpy. This phenomenon will be studied in future work. The irregular double helix structure in the crystalline structure zone also causes the heterogeneous structure in amylopectin-rich starch, and shows a higher phase transition temperature.

The viscosity value from RVA reflects the gel structure;⁴⁰ the final and setback viscosities also affect the edible quality and digestion property. For example, higher viscosity of starch gel may limit the entry rate of starch digestive enzyme to the starch inner zone. When starch is heated in excess water, the crystalline structure or double helical order of starch granules is destroyed, amylose and amylopectin dissolve in water and become entangled, so the amylose molecule entanglement in rice starch gel will affect the gel strength. When the temperature is reduced, the amylose is easy to retrograde and form hydrogen bonds between molecules, contributing to firm gels,¹⁴ so a higher final and setback viscosity is observed for amylose-rich starch.

4. Conclusions

The relationship between multi-scale structure and thermal properties of rice starch was examined in this work, which is important to starch-based food processing. The molecular and aggregation structures of Indica rice with different amylose content were studied by gel-permeation chromatography, high-performance anion-exchange chromatography, X-ray diffraction, and small-angle X-ray scattering. Thermal behavior was studied by differential scanning calorimetry and rapid visco-analysis.

Both GPC and HPAEC results show that the amylopectin from debranching rice starch shows bimodal distributions, rice starch with higher content of amylopectin possessed the highest molar- and weight-based ratio of fraction fa′ (DP 6–12) and lower molar-based ratios of fractions fb′₃ (DP ≥ 37), while amylose-rich starch shows different results. XRD and SAXS confirm that amylopectin-rich starch has the highest crystallinity and scattering intensity. DSC results show that amylopectin-rich starch has the highest onset and peak gelatinization temperatures; however, there are no significant differences in gelatinization enthalpy, which may be due to the irregular double helix. The viscosity value from RVA reflects the gel structure; amylose-rich starch shows higher molecular entanglement in starch gel and higher retrogradation ability, so it has higher peak and setback viscosities.

Conflict of interest

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgements

The financial support from the National Key Research and Development Program (2016YFD0400205-1-1) and NSFC (31301554) is gratefully acknowledged.

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