Physicochemical, functional, thermal and rheological characterization of starch from huauzontle seeds (Chenopodium berlandieri spp. nuttalliae)

Caracterización reológica, térmica, funcional y fisicoquímica del almidón de semillas de huauzontle (Chenopodium berlandieri spp. nuttalliae)

Melissa Assad-Bustillos^1,2, Mariana Ramírez-Gilly¹, Alberto Tecante¹, Leandro Chaires-Martínez³*

¹ Departamento de Alimentos y Biotecnología, Facultad de Química, Universidad Nacional Autónoma de México. 04510. Ciudad Universitaria. D.F. México.

³ Centro de Investigación en Alimentos. Instituto Tecnológico Superior de Álamo Temapache. 92750. Carretera Potrero del Llano-Tuxpan, km 6.5 Álamo, Veracruz, Mexico. *Author for correspondence (leandrochaires@yahoo.com.mx).

Received: May, 2014.
Approved: October, 2014.

Abstract

Huauzontle seeds (Chenopodium berlandieri spp. nuttalliae) are produced in the central part of Mexico but their use is limited to seedling process. Thus, in order to diversify their applications it is necessary to study their components such as proteins and starch. Therefore, the objective of this study was to extract and characterize the starch contained in the seeds of huauzontle by means of chemical and physical techniques. Analysis of the results showed 50 % extraction yield, 72.5 % starch purity, 5.32 % moisture, 1.09 % ash, 0.083 % fat, 11.4 % total nitrogen, and 4.13 % crude fiber. The amylose content was 10.5 %, which suggests that huauzontle starch gels could have a low tendency to retrograde. Swelling and solubility were similar to reported values for corn, lower than potato and higher than quinoa starches. The peak temperature of gelatinization was 68 °C. Pastes with 4 and 8 % (w/v) starch exhibited solid-like behavior attributable to amylose gelation with clear differences in dynamic moduli values and dependence with angular frequency when starch concentration increased. Non-Newtonian, shear-thinning behaviors with some degree of thixotropy that disappeared upon continuous shearing were observed. Laser diffraction data and SEM observations revealed association of very small (0.5-1.0 μm) starch granules into larger particles.

Key words: Chenopodium berlandieri, rheology, starch, viscoelasticity, microscopic structure.

Las semillas de huauzontle (Chenopodium berlandieri spp. nuttalliae) se producen en la parte central de México pero su uso se limita al proceso de producción de plántulas. Así, con el fin de diversificar sus aplicaciones es necesario estudiar sus componentes, como las proteínas y el almidón. Por lo tanto, el objetivo de este estudio fue extraer y caracterizar el almidón contenido en las semillas de huauzontle mediante técnicas químicas y físicas. El análisis de los resultados mostró 50 % de rendimiento de extracción, 72.5 % de pureza de almidón, 5.32 % de humedad, 1.09 % de cenizas, 0.083 % de grasa, 11.4 % de nitrógeno total y 4.13% de fibra cruda. El contenido de amilosa fue 10.5 %, lo cual sugiere que los geles del almidón de huauzontle podrían tener una tendencia baja a retrogradar. El hinchamiento y solubilidad fueron similares a los valores reportados para el maíz, menores que para papa y mayores que los almidones de quinua. La temperatura máxima de gelatinización fue 68 °C. Las pastas con 4 y 8 % (p/v) de almidón exhibieron un comportamiento semisólido atribuible a la gelificación de la amilosa con claras diferencias en los valores de módulos dinámicos y dependencia con frecuencia angular cuando aumentó la concentración de almidón. Hubo comportamientos pseudoplásticos no Newtonianos con cierto grado de tixotropía que desaparecieron tras continuo cizallamiento. Los datos de difracción laser y observaciones MEB revelaron una asociación de gránulos de almidón muy pequeños (0.5-1.0 μm) en partículas más grandes.

Palabras clave: Chenopodium berlandieri, reología, almidón, viscoelasticidad, estructura microscópica.

INTRODUCTION

The pseudocereal huauzontle (Chenopodium berlandieri spp. nuttalliae) is commercialized as a broccoli-like vegetable in several states of central México, and represents an alternative for profitable purposes (Partap et al., 1998). The main producing zones of huauzontle are in the state of Puebla, with approximately 3100 t year⁻¹ (SAGARPA, 2013). The edible part of the plant is the inflourescence but its seeds, which are used only for seedling process, present functional properties for the food industry due to the presence of antioxidants, proteins and starch, as it is the case of other pseudocereals (Aghamirzaei et al., 2013; Chaires et al., 2013). Therefore, in order to diversify the food applications of all of the huauzontle plant, it is necessary to characterize their components and to encourage their cultivation and use as an alternative to cereals. The fact that huauzontle starch can be extracted makes it available for food applications; however, its industrial potential remains untapped and it is important to understand the structural characteristics of starches in order to suggest further applications.

Starch is organized in discrete granules in most vegetable tissues, but it is particularly abundant in storage organs including roots/tubers, stems, seeds/ grains and fruits (Copeland et al., 2009). The complexity of starch biosynthesis produces variability in amylose and amylopectin molecules, which is reflected in the diversity of granule morphology. Variability in granule size and shape is associated with differences in functional properties such as gelatinization, retrogradation, solubility, swelling power, water-binding capacity, rheological behavior and pasting properties (Wang et al., 2010). For this reason, the tendency is to look for alternative sources to obtain starches exhibiting novel physicochemical and functional characteristics (Nwokocha and Williams, 2009). There are basic investigations on the properties of starch contained in pseudocereals plants like buckwheat (Fagopyrum esculentum) (Steadman et al., 2001), quinoa (Chenopodium quinoa) (Chauhan et al., 1992) and amaranth (Amaranthus spp.) (Calzetta et al., 2000), but none on the Mexican pseudocereal huauzontle. Thus, the objective of the present study was to evaluate swelling and solubility behavior, amylose content, gelatinization, morphology, particle size and rheological behavior of huauzontle seed starch.

MATERIALS AND METHODS

Starch extraction

The seeds were cleaned manually to remove foreign objects. Starch was isolated according to Lindeboom et al. (2005) and air-dried at 38 °C in a convection oven (Thermal Control, Genlab, Widnes, England).

Chemical analysis

The starch moisture, ash, total nitrogen (protein content calculated as nitrogen X 6.25), crude fat, crude fiber and carbohydrates were determined according to AOAC (1990) methods. Reducing sugars were determined by the dinitrosalicylic acid (DNS) method (Bernfeld, 1951).

Starch and amylose

Starch was determined by an enzymatic method using a Starch Assay Kit (Sigma-Aldrich, USA) based on the hydrolysis of starch to glucose catalyzed by α-tamylase and amyloglucosidase (Sigma-Aldrich, 2014). Amylose content was analyzed using an Amylose/Amylopectin Assay Kit (Megazyme, Ireland) based on the concanavalin A method (Yun and Matheson, 1990).

Swelling power and solubility

Starch paste was prepared at 4 % (w/v) by using a thermostatic bath (Polystat mod. 12101-50, Cole Parmer, USA) with a gradual heating program (1.5 °C min^-1) from 25 to 90 °C under constant stirring. The paste was kept at 90 °C for 10 min. Determinations were carried out as described by Leach et al. (1959).

Gelatinization and rheological behavior

The gelatinization properties of starch were determined using differential scanning micro-calorimetry (Micro-DSC 7-evo, Setaram Instruments, Caluire, France). Starch dispersions at 4 % (w/v) were placed in the sample cell. The samples were heated from 25 to 90 °C at a rate of 1.2 °C min⁻¹. Once the samples reached 90 °C they were maintained 10 min and then cooled to 25 °C at rate of 1.2 °C min⁻¹. Onset (T_onset) and peak (T_peak) temperatures, and enthalpy of gelatinization (AH) were determined. The rheological properties were analyzed for 4 and 8 % (w/v) starch pastes. The starch dispersions were heated in sealed tubes immersed in a water bath maintained at 99 °C for 30 min. The samples were agitated 3 min until pasting occurred. The pastes were removed and left at 25 °C and 1 h later the rheological properties were evaluated. Rheological measurements were carried out in a rheometer (Ares^® RFS III™, TA Instruments, USA) with serrated parallel plates geometry (25 mm in diameter and 1 mm gap). The storage modulus (G') and loss modulus (G") of the starch pastes were determined by small deformation oscillatory measurements in the zone of linear viscoelasticity, previously determined from strain sweep tests carried out at 25 °C and 6.28 rad s⁻¹. The variation of shear stress with shear rate was examined at 25 °C within a 0-140 s⁻¹ range. Two consecutive up and down shear rate loops, 6 min up and 6 min down, for each loop were carried out.

Particle size and particle size distribution of the starch granules were measured by laser light scattering (Mastersizer 2000, Malvern Instruments^®, UK) for 4 and 8 % (w/v) pastes. A polydisperse mode of analysis and a 300 mm lens were used. The starch was evenly dispersed in deionized water with magnetic agitation to attain an obscuration of 20-30 %. The particle size distribution was determined in triplicate, and the results were expressed as volume (%) occupied by starch granules (Tecante and Doublier, 1999). Granule micrographs were obtained with a JSM 35 Genie Scanning Electron Microscope (SEM). The starch was sprinkled onto a double-backed adhesive carbon tab stuck to a circular aluminum stub. The aluminum stub with the starch sample on it was placed in the vacuum chamber of a Polaron PS 3 sputter coater, after attaining a vacuum of 0.1-0.2 Torr and plasma current of 42 mA; the gold coating process was carried out for 140 s. The stub with gold-coated starch was then placed in the SEM chamber which was evacuated before the electron beam was turned on. A 10 kV/2.05 setting was used for the subsequent imaging on starch, and the aperture size was fixed at 3.

Statistical analysis

To verify the statistical significance between three measurements of each variable, means and standard deviation were determined (Fry, 1996).

RESULTS AND DISCUSSION

Chemical analysis and functional characteristics

Partial chemical composition and functional characteristics of starch are shown in Table 1. The starch yield of the huauzontle seeds (50 ±1.4 %) was close to Chenopodium quinoa (Chauhan et al., 1992), amaranth (Souci et al., 2000), and corn (Zea mays) (Ji et al., 2004); but lower than wheat (Triticum spp.) (Aguilar and Eckhoff, 2007) starches. Variability in yield values may have been affected by the structure of the source and the method used for extraction (Nwokocha and Williams, 2009). The moisture content (5.32±0.2 %) was low and within the acceptable range for marketing and storage (Wolfgang et al., 1999). Differences in starch moisture from several samples could be attributed to differences in drying and storage environment (Soni et al., 1993). The ash (1.09±0.1 %) and fat (0.083±0.2 %) content were slightly higher than quinoa and amaranth, but close to corn and wheat samples. The shelf life of flours depends largely on the fat content; thus, the lower the fat content the highest starch shelf life (Skrabanja et al., 2004).

Huauzontle seed starch had higher in protein content (11.4 ±0.4 %) than the values reported by Clerici et al. (2011) for Solanum lycocarpum (6.27 %) and Stevenson et al. (2006) 6.7 % for corn. Besides starch, protein content would be responsible for the textural characteristics of future huauzontle products, as was described for buckwheat and other grains (Skrabanja et al., 2004). Therefore, choosing the appropriate ratio between starch and protein content is important for designing and manufacturing products.

The presence of protein in huauzontle seed starch could be ascribed to non-separating protein from the matrix where the starch is embedded inside the grain (Ruales and Nair, 1994). By definition, starch granule-associated proteins are the proteins naturally positioned in and on starch granules. They are different from storage proteins and are bound tightly on the surface or as integrated constituents within the granule structure, or both (Baldwin, 2001). Some authors have tried to separate the soluble and insoluble fractions of protein from the starch-milk of amaranth and other sources. For example, Middlewood and Carson (2012) reported 32 % protein content from the starch-milk composition, and using microfiltration they obtained a starch-rich concentrate with low protein content.

Swelling and solubility patterns provide information about the nature of the associative bonding within the starch granule. The ratio of amylose and amylopectin in the starch granule and the manner in which they are arranged inside affect swelling and solubility of the starch (Beleia et al., 1980). The solubility of starch is dominated by the amylose content and amylopectin mainly influences the starch swelling power (Tester and Morrison, 1990). Starches such as quinoa, amaranth and huauzontle have reduced proportions of amylose and show low solubility when heated in excess water (Ahamed et al., 1996). For sources such as potato, 100 % solubility (Pomeranz, 1991) is associated with the easy bonding of water molecules to the free hydroxyl groups of amylose and amylopectin by hydrogen bonds, which could increase the absorption capacity and solubility (Singh et al., 1994; Ahamed et al., 1996). According to Kong et al. (2009), there was no correlation between amylose content and swelling power, but the correlation was negative with solubility index, as compared to several amaranth genotypes with 4.7 to 12.5 % amylose. For huauzontle seed starch, the results of amylose content, swelling power and solubility agree with values for K350 and R159 (Amaranthus cruentus L. from US) samples reported by Kong et al. (2009). Huauzontle seed starch swelling values (23.3± 1.37 g g⁻¹) are close to quinoa (Lindeboom et al., 2005) and corn (Sandhu and Singh, 2007), but different from potato starches (36.5-40.5 g g⁻¹) (Singh et al., 2006). Low swelling power of starches as in huauzontle seed starch may be attributed to the presence of a large number of crystal regions formed through the association between long amylopectin chains (Jiang et al., 2012). In pearl millet (Pennisetum glaucum) starches, values obtained for huauzontle seed starch can be considered as highly restricted as swelling power was below 16 g g⁻¹. Starches showing restricted swelling behavior are relatively stable against shearing action during cooking in water (Galvez and Resurreccion, 1992). Solubility of starch is an indicator of the degree of starch granules dispersion after cooking. The solubility could imply the amount of amylose leaching out from starch granule when swelling; therefore, the higher the solubility the higher will be the amylose leaching (Srichuwong et al., 2005).

Gelatinization properties

A typical DSC thermogram for a 4 % (w/v) dispersion of the huauzontle seed starch is shown in Figure 1. The DSC curve shows an endothermic peak which is attributed to the gelatinization process. The T_peak for huauzontle seed starch was 68.4±0.57 °C. The T_onset was 63.2±0.64 °C. For other pseudocereals, quinoa starch gelatinizes at a relatively low temperature (54.2-61.9 °C), which is similar to the T_peak of wheat and potato starch, but lower than for corn starch. Kong et al. (2009) found a wide range of variations in thermal parameters among 15 cultivars of amaranth: the highest T_peak (77.8 °C) was for cultivar K350 and the lowest (68.8 °C) for cultivar NO1 (Amaranthus hypochondriacus). The difference in T_peak among starches is attributed to the interplay of three factors: starch composition, molecular structure of the amylopectin and granule architecture.

The ΔH of huauzontle seed starch was 10.5 ± 0.54 J g⁻¹. Quinoa starch has a AH of 7.3-10.5 J g⁻¹(Inouchi et al., 1999), amaranth starch 15.0 to 18.4 J g⁻¹(Kong et al, 2009), corn starch 17.2-20.5 J g⁻¹, wheat starch 12.1 J g⁻¹, rice starch 14.2-16.3 J g⁻¹and potato starch 18.8 J g⁻¹(Zobel, 1984). The AH gives an overall measure of crystallinity (quality and quantity), and is regarded as an indicator of the loss of molecular order of the double helices that form the amylopectin crystallites due to hydrogen bond breaking within the granule (Hoover and Vasanthan, 1994; McPherson and Jane, 1999). Amylopectin plays a major role in starch granule crystallinity, the presence of amylose lowers the melting point of crystalline region and the energy for starting gelatinization (Flipse et al., 1996).

Rheological properties

The storage modulus G' was significantly greater than the loss modulus G" (Figure 2), and both moduli exhibited some frequency dependence (Figure 3) indicating solid-like characteristics (Nwokocha et al., 2010; Mandala, 2012). The G' of starch pastes is affected by the rigidity of starch granules (Han et al., 2002); besides, G' is positively correlated with amylose content and molecular mass (Case et al., 1998). The lineal viscoelasticity zone at 4 % concentration was 0.1 to 3.0 % strain, while at 8 % it was 0.1 to 10.0 % (Figure 2).

Figure 3 shows the variation of storage modulus (G') and loss modulus (G") with angular frequency. G' was higher than G" over all the frequency range with the separation between them becoming narrower as angular frequency increased, which is a characteristic of solid-like behavior. There are similar results for other starches from Lablab purpureus (Nwokocha et al., 2010).

During the first up-down cycle, an hysteresis loop was observed; for a given shear rate, upward shear stresses were greater than downward shear stresses, indicating some degree of thixotropy. However, on a second up-down cycle the hysteresis loop practically disappeared and the thixotropic behavior was no longer present. This behavior, commonly observed in starch pastes, is attributed to orientation of starch granules along the flow field when pastes are continuously sheared, which leads to destruction of the original granule accommodation at the beginning of the first up and down shear rate cycle. An anti-thixotropic loop was observed for chemically modified waxy corn starch, but it disappeared when pastes were continuously sheared (Tecante and Doublier, 1999). According to Izidoro et al. (2007), the knowledge of rheological parameters is important in industrial applications not only to determine the energy consumption to pump a fluid with greater viscosity, but also to solve problems with air incorporation, which causes difficulties in pump operation and with undesired reactions such as oxidation and contamination. Examination of the rheological properties of starches is an important step in the characterization and understanding of their functional properties.

Particle size and scanning electron microscopy

The particle size distribution was monomodal for 4 and 8 % (w/v) pastes, and bimodal for raw starch (Figure 5, left). The median diameter for raw starch, 4 and 8 % starch pastes was 19.1, 14.1 and 15.5 μm, respectively. Microscopic observations (Figure 5, A-B right) of the starch samples confirmed association as clusters such as that reported by Varriano-Marston and DeFransisco (1984), who observed aggregates of 18-20 μm in quinoa starch. Aggregates typical of most starches consist of small granules, such as quinoa, amaranth and cow cockle (Saponaria vaccaria) (Lorenz, 1990). Clusters have different size and morphology according to the processing, drying or milling; thus, Zhao and Whistler (1994) found spherical aggregates produced by spray drying of the sample. In the present study, air drying and an analytical mill of blades were used, resulting in block aggregates. Figure 5 (C-D right) shows the morphology of the huauzontle seed starch granules with a 0.5-1.0 μm size, and irregular and polygonal morphology typical of most small granule starches (Jane et al., 1994). The morphology and size observed were similar to those of quinoa and amaranth cultivars with diameters from 1.05 μm to 1.32 μm (Chauhan et al., 1992; Kong et al., 2009). In the present study, the granule surfaces were smooth and without pores, although the presence of broken and truncated granules is not considered in the quality standard of starches (Sriroth et al., 2000). The morphology of starch granules depends on the biochemistry of the chloroplasts or amyloplasts, as well as plant physiology (Singh et al., 2003). Moreover, several factors can affect the granules' properties, including environmental factors such as temperature, storage and cultural practices, thereby influencing the physicochemical and thermal properties of starch granules (Kaur et al., 2009).

CONCLUSIONS

Starch was extracted from huauzontle seeds with adequate yield and acceptable purity. The amylose content suggests that huauzontle starch gels could have a low tendency to retrograde. Pastes exhibited solid-like behavior due mainly to amylose gelation, but amylopectin-rich ghost remnants could act as suspended particle reinforcing the solid-like behavior of gels formed in the continuous phase, with clear differences in dynamic moduli values and dependence with angular frequency when starch concentration was increased. There was non-Newtonian shear-thinning behavior with some degree of thixotropy, as well as an association of very small starch granules into larger particles. These results are the first contribution to describing starch from huauzontle seeds.

ACKNOWLEDGEMENTS

The authors appreciate the financial support from the Consejo Nacional de Ciencia y Tecnología (CONACYT) through grant 101498.

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