Food Chemistry 218 (2017) 56–63

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Food Chemistry

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Physicochemical properties of maca starch ⇑ ⇑ Ling Zhang a, Guantian Li b, Sunan Wang c, Weirong Yao a, , Fan Zhu b, a School of Food Science and Technology, Jiangnan University, 1800 Lihu Avenue, Wuxi 214122, Jiangsu Province, China b School of Chemical Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand c Canadian Food and Wine Institute, Niagara College, 135 Taylor Road, Niagara-on-the-Lake, Ontario L0S 1J0, Canada article info abstract

Article history: Maca ( meyenii Walpers) is gaining research attention due to its unique bioactive properties. Received 22 May 2016 Starch is a major component of maca roots, thus representing a novel starch source. In this study, the Received in revised form 26 August 2016 properties of three maca starches (yellow, purple and black) were compared with commercially , Accepted 30 August 2016 , and potato starches. The starch granule sizes ranged from 9.0 to 9.6 lm, and the granules were Available online 31 August 2016 irregularly oval. All the maca starches presented B-type X-ray diffraction patterns, with the relative degree of crystallinity ranging from 22.2 to 24.3%. The apparent amylose contents ranged from 21.0 to Keywords: 21.3%. The onset gelatinization temperatures ranged from 47.1 to 47.5 °C as indicated by differential Maca (Lepidium meyenii Walpers) scanning calorimetry. Significant differences were observed in the pasting properties and textural param- Starch Thermal property eters among all of the studied starches. These characteristics suggest the utility of native maca starch in Pasting products subjected to low temperatures during food processing and other industrial applications. Enzymatic susceptibility Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction Finardi-Filho, 2009). The content is especially high and is similar to those of cereal grains such as wheat (85%) and Maca (Lepidium meyenii Walpers) belongs to the family Brassi- maize (70–75%) (Arendt & Zannini, 2013, chap. 1 & 2) and root caceae. It is a unique highland crop traditionally cultivated in the such as potato (76.6%) (Grommers & Krogt, 2009), cassava central of at elevations of 3500–4000 m above sea level (80%) (Zhu, 2015a), and sweet potato (80%) (Zhu & Wang, 2014). (León, 1964). There are 13 or more different ecotypes in cultiva- Previous studies have mainly focused on the extraction or tion. These can be distinguished by their root colors, which are physiological function of the bioactive components, including yellow, purple, white, gray, black, yellow/purple or white/purple. macamides (alkamides), macaenes, benzyl , sterols The yellow ecotype is the commonest cultivar (47.8%), and is also and fatty acids (Wang, Wang, McNeil, & Harvey, 2007). The resi- commercially preferred (Gonzales et al., 2006). It was recom- dues remaining after the extraction of bioactive compounds from mended as a safe edible food by the FAO in 1992, and has been maca roots may represent by-products and potential waste. How- promoted for global cultivation. For example, in recent years, China ever, the possible utility of the major component (starch) has not has adopted maca as an economic crop in the highlands of the south- been studied widely. Information on maca starch is scant, with western regions. Maca is traditionally used as a stamina-builder and only one report focused on one genotype (Rondán-Sanabria & fertility-promoter (Gonzales et al., 2003) because of its medicinal Finardi-Filho, 2009). Rondán-Sanabria and Finardi-Filho (2009) ingredients, which are beneficial for the regulation of metabolism, showed that the maca starch of one ecotype had small granules, hormonal secretion, memory improvement, and antidepressant and a low gelatinization temperature (47.6 °C), and produced firm, activity (Hermann & Heller, 1997, chap. 4). The medicinal ingredi- stable gels. This suggests that maca starch could be used for food ents are only minor components according to their relative content, and other industrial applications that require processing at low while the major components of dry maca root are temperature. Much more knowledge of the basic properties of (59–73%) (mainly starch), protein (10–18%), fiber (8.5%), and maca starch from different varieties is required before it can be lipids (2–5%) (Dini, Migliuolo, Rastrelli, Saturnino, & Schettino, commonly used in foods. The use of new starches from non- 1994; Hermann & Heller, 1997, chap. 4; Rondán-Sanabria & conventional sources could provide further desired functional properties for added-value food product development. The objective of this research was to characterize the physico- ⇑ Corresponding authors. chemical and functional properties of starches isolated from the E-mail addresses: [email protected] (W. Yao), [email protected] three maca genotypes (yellow, purple and black) that are being (F. Zhu). http://dx.doi.org/10.1016/j.foodchem.2016.08.123 0308-8146/Ó 2016 Elsevier Ltd. All rights reserved. L. Zhang et al. / Food Chemistry 218 (2017) 56–63 57 developed in the southwestern highland regions of China. Three repeated. The extracted starch was dried in an air-forced oven at commercially important starches from potato, cassava, and maize 40 °C for 24 h, and sealed in a screw-capped tube until use. were also employed as control samples for comparison. This knowledge of the basic properties of its starch will guide the com- 2.3. Determination of the chemical composition prehensive utilization of maca, and provide reference for further applications of the starch. The starches were analyzed for protein, lipid, and phosphorus contents according to AOAC official methods (methods 960.52, 920.39 and 923.03, respectively) (AOAC, 2000). The protein content 2. Materials and methods was calculated using a conversion factor of 6.25.

2.1. Materials and reagents 2.4. Starch granule morphology

The maca roots of three genotypes of different colors (yellow, The morphology of starch granule was investigated using a purple and black) were obtained from Yunnan province, China. Polarize light microscope (Leica DMRE, Germany) and a scanning Potato was obtained from a local New Zealand market (Countdown electron microscopy (SEM) (S-3400N, Hitachi High-Technologies, Supermarkets). Two types of maize starch (Melogel and GELOSE Japan). Samples were coated with palladium–gold. Images of 50) were obtained from Ingredion ANZ Pty Ltd. (Auckland, New starch granules were obtained at an accelerating voltage of Zealand). Maize starch (Melogel) was used as the reference sample, 5.0 kV at various magnifications. and GELOSE 50 is a type of maize starch with an apparent amylose content of 50%. Commercial cassava starch was obtained from a 2.5. Particle size distribution local supermarket (Mayushan Food Co., Ltd, Taiwan). Pancreatic a-amylase (PPA, EC 3.2.1.1, type 1A) was purchased from Sigma- The size distribution of the starch granules was determined Aldrich Chemical Co. (Auckland, New Zealand). Phenol, sulfuric using a Mastersizer 2000 particle size analyzer (Malvern Instru- acid and Dimethyl sulfoxide (DMSO) were obtained from Sigma- ments Ltd., Worcestershire, UK). Starch samples (100 mg, dry Aldrich Chemie GmbH (Deisenhofen, Germany), Scharlau (Barce- weight basis) were dispersed in 10 mL double-deionized water lona, Spain) and Avantor Performance Materials Inc. (PA, USA), and the mixture was mixed vigorously for 10 min using a vortex respectively. All other reagents and chemicals were obtained from mixer. Then the starch particle size was measured at a speed of ECP Ltd. (Auckland, New Zealand). 2100 r/min.

2.6. X-ray diffraction analysis (XRD) 2.2. Starch isolation XRD was performed using an Empyrean X-ray diffractometer Starch was isolated according to previous method (Annor, (PANalytical, Netherlands) according to a published method Marcone, Bertoft, & Seetharaman, 2014) with some modifications. (Lopez-Rubio, Flanagan, Gilbert, & Gidley, 2008) with some modi- Briefly, dry maca roots (500 g) were thoroughly washed, and then fications. Starches were equilibrated over a 44% potassium carbon- macerated in a beaker using 1:2 (w/v) (maca root to deionized ate (K2CO3) solution at room temperature for two weeks before water) for 48 h, manually peeled, and further homogenized in a analysis. mixer at full speed for 40 s with cold deionized water. The slurry The diffractometer was equipped with a long copper fine-focus was sieved. The supernatant was collected, and the insolubles were tube and the operating conditions were: target voltage, 45 kV; cur- re-suspended in water and further homogenized four times. Then rent, 40 mA; step size, 0.01°; receiving slit width, 0.1 nm; scan step the slurry was stirred using 2 L of sodium borate buffer time, 51 s; and scanning range, 4–40° 2h.

(12.5 mM, pH 10), containing 0.5% SDS (w/v) and 0.5% Na2S2O5 The crystalline and amorphous areas were determined accord- (w/v) for 30 min to remove the proteins, the residue was then ing to a previous method (Hayakawa, Tanaka, Nakamura, Endo, & recovered by centrifugation at 3000g for 15 min. The above Hoshino, 1997). Crystallinity was calculated as follows: Degree of extraction step was repeated. The resulting residue was washed crystallinity (%) = Ac 100/(Ac + Aa), where Ac is the total area of several times with deionized water and recovered by centrifuga- the crystalline peaks, Aa is the amorphous area of the tion at 3000g for 15 min. The starch slurry was passed through diffractogram. four layers of cheesecloth and then through 140 lm nylon mesh. The slurry was centrifuged at 3000g for 15 min again, and the 2.7. Apparent amylose content brown layer formed on top of the starch layer was removed with a spatula. Then the starch was suspended in deionized water and The apparent amylose content (AAM) was determined using centrifuged. These steps were repeated three more times to iodine binding method described previously (Li, Wang, & Zhu, remove all the brown particles from the starch fraction. The iso- 2016). lated starch was then dried in an oven at 35 °C for 24 h, and then sealed in a screw-capped tube until use. 2.8. Swelling power (SP) and water solubility index (WSI) Potato starch was extracted using a modification of a previous procedure (Collado, Mabesa, & Corke, 1999). Briefly, tubers were SP and WSI were determined following a modified method (Li & thoroughly washed, peeled and cut into 2–3 cm cubes, further Yeh, 2001). Starch (W0 150 mg, dry weight basis) was directly macerated in a blender using 1:1 w/v (potato root to deionized weighed into a plastic centrifuge tube, and deionized water water) for 45 s at medium speed. The starch slurry was passed (10 mL) was added into the tube. Then the capped tubes were incu- through four layers of cheesecloth. Then the residue was bated in 45 °C, 55 °C, 65 °C, 75 °C, 85 °C and 95 °C water baths for re-suspended in deionized water (1:0.5 w/v) and blended for 30 min, with frequent mixing at about 2 min intervals by placing 45 s. This step was repeated, and the suspension of sediment was them on a vortex mixer for 5 s. The tubes were then cooled to room mixed and passed through a 140 lm nylon mesh. All the material temperature in an iced water bath and centrifuged at 3000g for retained by the mesh was washed several times with deionized 30 min. The supernatant was poured out from the tube. A cloudy water and kept in a refrigerator to settle. The last step was portion was poured out along with the clear supernatant and 58 L. Zhang et al. / Food Chemistry 218 (2017) 56–63 considered as part of the supernatant. The materials that adhered 7.5 min, then held at 95 °C for 5 min before cooling linearly to to the wall of the tube were considered as the sediment, and these 50 °C in 7.5 min, and finally held at 50 °C for 2 min. The total run were weighed (Ws). The supernatant was then dried to constant time was 27 min. The peak time (Ptime), peak viscosity (PV), cool weight (W1) in an air-forced oven at 100 °C. The WSI and SP were paste viscosity (CPV), hot paste viscosity (HPV), and the derivative expressed as follows: parameters, breakdown (BD = PV HPV) and setback  (SB = CPV HPV) were recorded. W WSI ¼ 1 100% W0 2.13. Gel textural analysis W SP ¼ s ðg=gÞ W0 ð100% WSIÞ After pasting analysis, the starch gel was transferred to a glass tube, sealed and kept for 24 h at 4 °C before analysis. Gel textural properties were studied using a TA-XT texture analyzer (Stable 2.9. Amylose leaching Micro Systems Ltd., Surrey, UK) under Texture Profile Analysis mode (TPA) according to a previous method (Li et al., 2016). Amylose leaching was determined using a method from Varatharajan et al. (2011). Starch (20 mg, dry weight basis) was directly weighed into a screw-capped test tube, and 10 mL deion- 2.14. Statistical analysis ized water was added. The tubes were heated at 45 °C, 55 °C, 65 °C, 75 °C, 85 °C and 95 °C for 30 min, during which the tubes were sha- All analyses were determined in triplicate. Data were presented ken by hand every 5 min to suspend the starch slurry. Then the as means and were analyzed using SPSS 22.0 (IBM Corporation, NY, tubes were cooled at ambient temperature and centrifuged at USA). The data were labelled alphabetically and p < 0.05 was con- 3000g for 30 min. The supernatant liquid (1 mL) was withdrawn sidered as statistically significant. and its amylose content was determined as described in 2.7. Amy- lose leaching was calculated as the percentage of amylose leached 3. Results and discussion per 100g of dry starch. 3.1. Chemical composition 2.10. Enzymatic susceptibility The chemical compositions of the isolated maca starches in The enzymatic susceptibility of each starch was analyzed comparison with maize, cassava and potato starches are shown according to a previous description (Li et al., 2016; Varatharajan in Table 1. The protein content of the maca starches ranged from et al., 2011). Starch (10 mg, dry weight basis) was added to 5 mL 0.07 to 0.10%, lower than those of maize starch (0.15%) and cassava deionized water and 4 mL phosphate buffer (0.1 mol/L, pH 6.9) l starch (0.16%) but higher than that of potato starch (0.04%). The containing NaCl (0.006 mol/L). Then, 10 L PPA suspensions low protein content may reflect the efficient isolation method for (1.8 units/mg starch) were added after the slurry was pre- purifying the starch. No lipid content was detected in any of the ° warmed for 30 min at 37 C and gently vortexed. The digestion starches. This is consistent with the low lipid contents generally reaction was terminated by adding 2 mL of 95% ethanol and the found in the starch granules of tuber and root starches (Hoover, samples were analyzed after 3, 6, 12, 24, 48 and 72 h of incubation 2001). Another important component of starch is phosphorus. ° at 37 C in a shaking water bath. The hydrolyzate was recovered by The phosphorus contents of the three maca starches varied centrifugation (2000 g, 5 min) of the mixture. Aliquots of the between 159.7 and 214.0 mg/kg. This variation among the yellow, supernatant were analyzed for soluble carbohydrate according to Ò purple and black maca starches supports the argument that the the modified phenol–sulfuric acid method using Corning 96- phosphorus content of starch is very susceptible to growing condi- well half-area microplates (Corning Incorporated, Corning, NY, Ò tions and the botanical source (Raeker, Gaines, Finney, & Donelson, USA) and an EnSpire Multimode Plate Reader (PerkinElmer Inc, 1998). The phosphorus contents of the maca starches are similar to Waltham, MA, USA). Standard curves were measured using a gradi- that of maize starch (136.3 mg/kg) and higher than that of cassava ent concentration of glucose solution. The degree of hydrolysis was starch (57.2 mg/kg). Potato starch showed the highest phosphorus expressed as grams of glucose per 100 g starch. content (548.8 mg/kg). The phosphorus contents of these control samples were similar to the results of previous reports 2.11. Thermal properties (Kasemsuwan & Jane, 1996). It is important to note that a high phosphorus content can contribute to the high viscosity of starch Starch gelatinization was studied using a differential scanning (Moorthy, 2002). calorimeter (DSC) (TA Instruments, Q1000 Series, New Castle, The apparent amylose contents of maca, maize, cassava, and USA) according to a method at Zhu, Yang, Cai, Bertoft, and Corke potato starches are summarized in Table 1. For the three maca (2011). Four thermal parameters were recorded: the onset (To), starches, these were 21.0% (yellow), 21.3% (purple) and 21.1% peak (Tp), conclusion (Tc) temperatures, and the enthalpy change (black), respectively. The amylose contents of the maca starches of gelatinization (DH). showed no significant difference. These results were similar to a previous study on maca starch of one genotype, with an amylose 2.12. Pasting analysis content of 20.45% (Rondán-Sanabria & Finardi-Filho, 2009). The maca starches had lower amylose contents than maize starch A rheometer (Anton Paar Physica MCR 301 stress controlled, (24.2%) and potato starch (25.0%), while there was no significant Austria) was used to analyze the pasting properties of the starch difference between maca and cassava starch (21.9%). The amylose according to a previous method (Zhu et al., 2011). Starch (2.0 g, contents of the maca starches were lower than those reported for dry weight basis) and deionized water (20 mL) were mixed to yield other Andean tubers, such as oca (Oxalis tuberosa), olluco (Ullucus a total constant weight of 22.0 g in the rheometer sample canister. tuberosus) and mashua (Tropaeolum tuberosum)(Valcárcel- Starches were analyzed as follows: the samples were held at an ini- Yamani, Rondán-Sanabria, & Finardi-Filho, 2013). Amylose content tial temperature of 50 °C for 5 min, heated linearly to 95 °Cin has a significant effect on the physicochemical properties of starch, L. Zhang et al. / Food Chemistry 218 (2017) 56–63 59

Table 1 Chemical composition, particle size and apparent amylose content and crystallinity of maca starches.

Starch Protein (%) Phosphorus (mg/kg) Mean particle size (lm) AAM (%) Crystallinity (%) Yellow maca 0.09b 159.7cd 9.0e 21.0b 23.2e Purple maca 0.10b 184.1c 9.0e 21.3b 24.3d Black maca 0.07c 214.0b 9.6d 21.1b 22.2f Maize 0.15a 136.3d 14.9c 24.2a 34.5a Cassava 0.16a 57.2e 16.4b 21.9b 33.1b Potato 0.04d 548.8a 44.8a 25.0a 28.4c

AAM: Apparent amylose content; values in each column followed by the same letter are not significantly different (p < 0.05). including its pasting, retrogradation and swelling behavior (Zhu, yam starch (Zhu, 2015b). The general morphology of the maca 2015a). starch granules found in this study were similar to those of the maca starch of one genotype reported by Rondán-Sanabria and 3.2. Morphology of starch granules Finardi-Filho (2009) and oca starch (Santacruz, Koch, Svensson, Ruales, & Eliasson, 2002), i.e., other starches from Andean root Microphotographs of granules of the three maca starches are crops. shown in Fig. 1. The starch granules of the three maca genotypes The particle size distributions of the three maca starches and had similar irregular oval shapes, markedly different from those maize, cassava and potato starches are shown in Fig. 2A and sum- of maize, cassava and potato starch (Mishra & Rai, 2006). There marized in Table 1. All of the starches presented mono-modal size are small fissures on the surfaces of maca starches, similar to distributions. The mean particle sizes of maca starches ranged from

Fig. 1. Polarize microscope and Scanning electron microscope (SEM) images of maca starches. 60 L. Zhang et al. / Food Chemistry 218 (2017) 56–63

28.4%, respectively (Table 1). The crystallinity of the three maca starches showed significant differences, and followed the order purple maca > yellow maca > black maca. This may be due to the differences in the chain-length distribution of their amylopectins (Hoover, 2001). The crystallinity of maca and potato starches is much lower than that of maize and cassava starches. Previous reports indicated that B-type starches tended to have lower levels of crystallinity (15–28%) than A-type starches (33–45%) (Zobel, 1988).

3.4. Swelling power (SP) and water solubility index (WSI)

The SP and WSI of maca, maize, cassava, and potato starches at different temperatures (45, 55, 65, 75, 85 and 95 °C) were mea- sured (Fig. 3). The swelling power (Fig. 3A) and water solubility (Fig. 3B) of the starches were positively correlated with the tem- perature from 45 °Cto85°C. Compared with purple and black maca, the SP of yellow maca was higher, indicating less resistance to swelling, may be due to the presence of weaker bonding forces maintaining the granule structure. The SP values of maca, cassava and potato starches were significantly higher than that of maize starch. This agreed with previous results which indicated that cer- eal starch swelled less than tuber and root starches (Li & Yeh, 2001). The SP of the three maca starches (Fig. 3A) showed different swelling patterns than those of maize, cassava and potato starches. The SP of the maca starches dropped at 95 °C. A similar drop in swelling was also observed in a previous study of maca starch (Rondán-Sanabria & Finardi-Filho, 2009) and other starches, such as and sweet potato starch (Li & Yeh, 2001), and this might be due to a loss of granule structure during heating at higher temperature. All of the studied starches showed similar WSI values at 55 °C. From 55 to 85 °C, maize starch presented the lowest WSI. The lower WSI of maize starch could have been caused by its more compact structure and higher crystallinity than tuber and root Fig. 2. Particle size distribution of maca, maize, cassava and potato starches (A); X- ray diffractogram of maca, maize, cassava and potato starches (B). starches, typical of cereal starches (Jane, 2006; Mishra & Rai, 2006).

9.0 to 9.6 lm, and the individual sizes ranged from 2 to 20 lm. 3.5. Amylose leaching Wide variability in the size of the investigated starch granules has been observed, and the average diameters of these starch Amylose leaching (AML) of maca, maize, cassava, and potato granules ranged from 9.0 to 44.8 lm. The mean granule diameters starches at different temperatures (45, 55, 65, 75, 85 and 95 °C) of the starches in this study followed the following order: is shown in Fig. 3C. The AML of all evaluated starches increased potato > cassava > maize > black maca > yellow maca purple with increasing temperature, and especially sharply between 75 maca. The sizes of the maca starch granules are in agreement with and 95 °C. The yellow maca starch presented greater AML than a previous report on maca starch of one genotype (Rondán- the other starches. The three maca starches had similar amylose Sanabria & Finardi-Filho, 2009). Maca starch granules are smaller contents, and the differences in their AML may be attributable to than those of other Andean root crops such as biri (Canna edulis) the different amylose–amylose and amylose–amylopectin chain and oca, which vary between 35 and 101 lm, and 22 and 55 lm, interactions (Naguleswaran, Vasanthan, Hoover, & Liu, 2010). The respectively (Santacruz et al., 2002). AML of maca starches started at a lower temperature (45 °C) than did that of maize, cassava and potato starch, and the AML of maize starch was detectable only at temperatures exceeding 65 °C. The 3.3. X-ray diffraction analysis (XRD) absence of AML in maize starch at low temperature may have been caused by its more compact structure and higher crystallinity than The wide-angle X-ray diffraction patterns of maca, maize, cas- tuber and root starches, typical of cereal starches (Jane, 2006; sava and potato starches are shown in Fig. 2B. The three maca Mishra & Rai, 2006). For starches with similar amylose contents, starches and potato starch presented typical B-type X-ray diffrac- small-granule starches have been shown to leach more amylose tion pattern with peaks at 5.5, 17, 22 and 24° 2h angles. Maize from their intact granules than do their larger-granule counter- and cassava starches presented typical A-type X-ray diffraction parts at temperatures of 55 °C and higher (Lindeboom, Chang, & patterns with peaks at 15 and 23° and a doublet peak at 17 and Tyler, 2004). 18° 2h angles. The diffraction patterns may be affected by environ- mental factors, crop developmental stage and harvesting season 3.6. Enzymatic susceptibility (Zhu, 2015a). The maca crops used in this study were grown in similar environments in Yunnan province, Southwestern China. The patterns of hydrolysis (72 h) of maca, maize, cassava and The crystallinity showed significant differences among the potato starches by PPA are shown in Fig. 3D. The extent and rate maca, maize, cassava and potato starches, being 23.2 (yellow of hydrolysis among the three maca starches followed the order maca), 24.3 (purple maca), 22.2 (black maca), 34.5, 33.1 and black maca > yellow maca > purple maca. This may be attributa- L. Zhang et al. / Food Chemistry 218 (2017) 56–63 61

Fig. 3. Swelling power of maca, maize, cassava and potato starches (A); water solubility index of maca, maize, cassava and potato starches (B); amylose leaching of maca, maize, cassava and potato starches (C); enzymatic susceptibility of maca, maize, cassava and potato starches (D). ble to the differences in their crystallinity (Table 1). In the first (yellow > purple black) did not exactly match the crystallinity 24 h, maca and cassava starches were hydrolyzed to a greater order (purple > yellow black) (Table 1). This mismatch may have extent, whereas maize starch displayed the lowest extent of arisen because differences in crystallinity among starches are not hydrolysis. There was an initial steep rise in the hydrolysis rate only affected by the degree of crystallite perfection, but also by of purple maca starch. This rise could have been due to the small how the crystallites are oriented (Maaran, Hoover, Donner, & Liu, granules of this maca starch, with a higher surface-to-volume 2014). The gelatinization temperatures of the maca starches agreed ratio (Table 1)(Kulp, 1973). From 24 to 48 h, maize starch with those reported in previous studies (Rondán-Sanabria & showed a greater extent of hydrolysis than maca starches. The Finardi-Filho, 2009; Torres, Troncoso, Díaz, & Amaya, 2011), but hydrolysis of all starches reached a plateau after 48 h. At the later were lower than those of the Andean root starches oca, olluco stages of hydrolysis, the enzymes mainly attack the crystalline and mashua (Valcárcel-Yamani et al., 2013). The variation in the regions of the granule, the crystal structures of which are directly thermal properties of these Andean crop starches may be attribu- related to the fine structure of amylopectin. The susceptibility of table to the different botanical sources and growing conditions. native starch granules to PPA is influenced by several factors, Compared to maize and cassava starches, the temperatures of such as granule size, amylose content, crystalline perfection and maca and potato starches were lower because type B starches tend the chain-length distribution of the amylopectin units to have lower gelatinization temperatures (Zobel, 1988). (Varatharajan et al., 2011). The hydrolysis of A-type starch is much faster than that of B-type starch granules due to the greater Table 2 presence of structural defects (Jane, 2006). Thermal properties of maca starches.

Starch To (°C) Tp (°C) Tc (°C) DH (J/g)

d e cd c 3.7. Thermal properties Yellow maca 47.5 51.4 57.8 14.6 Purple maca 47.1e 52.1d 58.0c 14.3c Black maca 47.2e 50.8f 57.4d 14.2c a a a bc The gelatinization temperatures (onset, To, peak, Tp and conclu- Maize 68.6 72.5 77.5 14.9 b b a a sion, Tc) and gelatinization enthalpy (DH) for maca, maize, cassava Cassava 60.3 67.8 77.3 16.7 c c b b and potato starches are presented in Table 2. Considerable variabil- Potato 58.2 61.2 67.9 15.6 ity in the values was observed. Compared to maize, cassava and To: onset temperature; TP: peak temperature; Tc: conclusion temperature; DH: potato starches, maca starches generally had lower gelatinization enthalpy of gelatinization; Values in each column followed by the same letter are not significantly different (p < 0.05). temperatures (To, Tp and Tc). The order of gelatinization temperature 62 L. Zhang et al. / Food Chemistry 218 (2017) 56–63

Table 3 Pasting and gel texture properties of maca starches.

PV(Pa s) HPV (Pa s) BD (Pa s) CPV (Pa s) SB (Pa s) Ptime (min) HD (g) ADH (g s) COH Yellow maca 5.25b 1.54d 3.72b 3.32c 1.79b 10.1c 21.1de 141cd 0.57bc Purple maca 4.12d 1.64c 2.49d 3.33c 1.70c 11.5b 25.0cd 130d 0.58bc Black maca 4.65cd 2.20b 2.45d 3.94b 1.74c 12.0a 34.3b 155c 0.62ab Maize 2.83e 1.50e 1.33e 3.08d 1.58d 12.1a 48.8a 245a 0.42d Cassava 4.38c 1.28f 3.10c 2.58e 1.30e 10.0c 18.5e 105e 0.56c Potato 14.75a 2.45a 12.30a 4.75a 2.30a 8.3d 27.5c 177b 0.65a

PV: peak viscosity; HPV: hot paste viscosity; BD: breakdown; CPV: cool paste viscosity; SB: setback; Ptime: peak time; HD: hardness; ADH: adhesiveness; COH: cohesiveness; values in each column followed by the same letter are not significantly different (p < 0.05).

Gelatinization enthalpy (DH) is an indication of the loss of exhibited the highest ADH, and the tuber and root starches the low- molecular (double-helical) order during gelatinization. The DH val- est. The COH values of the three maca starches were slightly higher ues for the three maca starches were similar (average 14.4 J/g), and than those of cassava and maize starch but lower than potato starch. were higher than values previously reported (6.22 J/g and 10.6 J/g) The differences in textural properties can be partially attributed to (Rondán-Sanabria & Finardi-Filho, 2009; Torres et al., 2011). No the lower amylose content of maca and cassava starches (Table 1). significant difference was observed in DH between starches from Native starch with a greater amylose content tends to develop a maca and maize. Among all of the studied starches, the DH of cas- stronger gel because the re-ordering of amylose is responsible for sava was the highest, indicating the formation of longer and more the initial retrogradation (Ai & Jane, 2015). Other factors such as double helices by the amylopectin external chains (Annor et al., the chain length of amylopectin may also play a role (Mua & 2014). Factors including granule size, amylose content, amy- Jackson, 1997). lopectin structure, and crystal structure (as revealed by XRD pat- terns) may also affect DH (Moorthy, 2002). 4. Conclusions

3.8. Pasting analysis Native non-conventional starches isolated from three geno- types of maca (Lepidium meyenii Walpers) presented variability in The pasting properties of the three maca starches in comparison their physicochemical and functional properties. Three maca with those of maize, cassava and potato starches are shown in starches exhibited similar compositional and physicochemical Table 3. Significant differences were observed in the pasting prop- properties among themselves, but have distinct properties com- erties among all of the starches, including among the three maca pared with the commercially important starches derived from starches. Yellow maca starch had the highest PV and BD, while potato, maize, and cassava. Maca starch is easy to gelatinize. It black maca starch had the highest CPV and Ptime, implying high sta- has a high degree of swelling and water solubility, high pasting vis- bility during cooking and shearing as an easy-to-cook starch cosity, low resistance towards shear and a high tendency to ret- (Valcárcel-Yamani et al., 2013). Recall that there was little differ- rogradation. Further research should thus focus on the ence in the amylose content and granule size of the maca starches relationships between the molecular structures and physicochem- (Table 1). The differences in the pasting properties could, however, ical properties of maca starches. be due to the molecular structure of amylopectin (Srichuwong & The data obtained in this study suggest that maca starch may be Jane, 2007), which remains to be studied. The SB values of the maca useful as a specialty starch in the food and non-food industries. Its starches were significantly higher than those of maize and cassava properties are especially suitable for products subjected to low- starches. The CPV values of the maca starches were higher than temperature processing. The high viscosity of yellow maca starch, those of maize and cassava starches and lower than potato starch. which is the most common genotype in China, would be valuable Potato starch had the highest PV, which can be attributed to the in many areas of the food industry, especially where high thickening high phosphate monoester content (Hoover, 2001). Maize starch power is preferred. The low viscosity of purple maca starch may be had the lowest PV (2.83 Pa s) and BD (1.33 Pa s). The various very useful in the paper-making industry, where lower viscosity is factors affecting the pasting properties include amylose content, desired. The high firmness of the black maca starch gel may be amylose and amylopectin structures, granular architecture, and the exploited through use as a jellifying agent in refrigerated foods. minor components such as phosphate (Srichuwong & Jane, 2007).

Acknowledgements 3.9. Gel textural analysis

The author would like to thank Associate Professor Yacine The textural parameters hardness (HD), adhesiveness (ADH) and Hemar from the University of Auckland for kindly provided the cohesiveness (COH) were obtained from texture profile analysis access to the facility for particle size and pasting analysis, and (TPA), and are shown in Table 3. HD expresses the firmness of the Dongxing Li for assistance on lab works. This research was sup- starch gel. ADH expresses the ability to adhere to other objects. ported by National Key Technology R&D Program in the 12th Five COH expresses the extent to which the starch gel structure is dis- Year Plan of China (No. 2014BAD04B03), Grain Industry Research rupted during first compression (Corke & Wu, 2000). The starch Special Funds for Public Welfare Projects (No. 201513006-03), gel texture of the three maca starches was similar, probably due to China Scholarship Council and Collaborative Innovation Center of their similar amylose contents (Table 1)(Hoover & Hadziyev, Food Safety and Quality Control in Jiangsu Province. 1981). However, significant differences were observed in the textu- ral parameters among all of the studied starches. Maize starch pre- sented the highest HD (48.8 g), followed by black maca (34.3 g), References potato starch (27.5 g), purple maca (25.0 g), yellow maca (21.1 g), and cassava starch (18.5 g). The ADH of the starches varied from Ai, Y. F., & Jane, J. L. (2015). Gelatinization and rheological properties of starch. Starch/Stärke, 67, 213–224. 105 to 245 g s, and followed the order maize > potato > black Annor, G. A., Marcone, M., Bertoft, E., & Seetharaman, K. (2014). Physical and maca > yellow maca purple maca > cassava. Maize starch thus molecular characterization of millet starches. Cereal Chemistry, 91, 286–292. L. Zhang et al. / Food Chemistry 218 (2017) 56–63 63

AOAC (2000). Official methods of analysis. Washington, DC: Association of Official Maaran, S., Hoover, R., Donner, E., & Liu, Q. (2014). Composition, structure, Analytical Chemists. morphology and physicochemical properties of lablab bean, navy bean, rice Arendt, E. K., & Zannini, E. (2013). Cereal grains for the food and beverage industries. bean, tepary bean and velvet bean starches. Food Chemistry, 152, 491–499. Cambridge: Woodhead Publishing Limited. Mishra, S., & Rai, T. (2006). Morphology and functional properties of corn, potato Collado, L. S., Mabesa, R. C., & Corke, H. (1999). Genetic variation in the physical and tapioca starches. Food Hydrocolloids, 20, 557–566. properties of sweet potato starch. Journal of Agricultural and Food Chemistry, 47, Moorthy, S. N. (2002). Physicochemical and functional properties of tropical tuber 4195–4201. starches: A review. Starch/Stärke, 54, 559–592. Corke, H., & Wu, H. X. (2000). Genetic variation in thermal properties and gel Mua, J. P., & Jackson, D. S. (1997). Relationships between functional attributes and texture of Amaranthus starch. In: International Symposium on Cassava, Starch molecular structures of amylose and amylopectin fractions from corn starch. and Starch Derivatives, Guangxi, China. Journal of Agricultural and Food Chemistry, 45, 3848–3854. Dini, A., Migliuolo, G., Rastrelli, L., Saturnino, P., & Schettino, O. (1994). Chemical Naguleswaran, S., Vasanthan, T., Hoover, R., & Liu, Q. (2010). Structure and composition of Lepidium meyenii. Food Chemistry, 49, 347–349. physicochemical properties of palmyrah (Borassus flabellifer L.) -shoot Gonzales, G. F., Córdova, A., Vega, K., Chung, A., Villena, A., & Góñez, C. (2003). Effect starch grown in Sri Lanka. Food Chemistry, 118, 634–640. of Lepidium meyenii (Maca), a root with aphrodisiac and fertility-enhancing Raeker, M. Ö., Gaines, C. S., Finney, P. L., & Donelson, T. (1998). Granule size properties, on serum reproductive hormone levels in adult healthy men. Journal distribution and chemical composition of starches from 12 soft wheat cultivars. of Endocrinology, 176, 163–168. Cereal Chemistry, 75, 721–728. Gonzales, C., Rubio, J., Gasco, M., Nieto, J., Yucra, S., & Gonzales, G. F. (2006). Effect of Rondán-Sanabria, G. G., & Finardi-Filho, F. (2009). Physical–chemical and functional short-term and long-term treatments with three ecotypes of Lepidium meyenii properties of maca root starch (Lepidium meyenii Walpers). Food Chemistry, 114, (MACA) on spermatogenesis in rats. Journal of Ethnopharmacology, 103, 492–498. 448–454. Santacruz, S., Koch, K., Svensson, E., Ruales, J., & Eliasson, A. C. (2002). Three Grommers, H. E., & Krogt, D. V. D. (2009). Potato starch: Production, modification underutilised sources of starch from the Andean region in Ecuador Part I. and uses. In J. BeMiller & R. Whistler (Eds.), Starch: Chemistry and technology Physico-chemical characterisation. Carbohydrate Polymers, 49, 63–70. (3rd ed., pp. 520). San Diego: Academic Press. Srichuwong, S., & Jane, J. L. (2007). Physicochemical properties of starch affected by Hayakawa, K., Tanaka, K., Nakamura, T., Endo, S., & Hoshino, T. (1997). Quality molecular composition and structures. Food Science and Biotechnology, 16, characteristics of waxy hexaploid wheat (Triticum aestivum L.): Properties of 663–674. starch gelatinization and retrogradation. Cereal Chemistry, 74, 576–580. Torres, F. G., Troncoso, O. P., Díaz, D. A., & Amaya, E. (2011). Morphological and Hermann, M., & Heller, J. (1997). Andean roots and tubers: Ahipa, arracacha, maca and thermal characterization of native starches from Andean crops. Starch/Stärke, yacon. Rome: International Genetic Resources Institute. 63, 381–389. Hoover, R. (2001). Composition, molecular structure, and physicochemical Valcárcel-Yamani, B., Rondán-Sanabria, G. G., & Finardi-Filho, F. (2013). The properties of tuber and root starches: A review. Carbohydrate Polymers, 45, physical, chemical and functional characterization of starches from Andean 253–267. tubers: oca (Oxalis tuberosa Molina), olluco (Ullucus tuberosus Caldas) and Hoover, R., & Hadziyev, D. (1981). The effect of monoglycerides on amylose mashua (Tropaeolum tuberosum Ruiz & Pavón). Brazilian Journal of complexing during a potato granule process. Starch/Stärke, 33, 346–355. Pharmaceutical Sciences, 49, 453–464. Jane, J. L. (2006). Current understanding on starch granule structures. Journal of Varatharajan, V., Hoover, R., Li, J. H., Vasanthan, T., Nantanga, K. K. M., Seetharaman, Applied Glycoscience, 53, 205–213. K., et al. (2011). Impact of structural changes due to heat-moisture treatment at Kasemsuwan, T., & Jane, J. L. (1996). Quantitative method for the survey of starch different temperatures on the susceptibility of normal and waxy potato phosphate derivatives and starch phospholipids by 31P nuclear magnetic starches towards hydrolysis by porcine pancreatic alpha amylase. Food resonance spectroscopy. Cereal Chemistry, 73, 702–707. Research International, 44, 2594–2606. Kulp, K. (1973). Characteristics of small-granule starch of flour and wheat. Cereal Wang, Y. L., Wang, Y. C., McNeil, B., & Harvey, L. M. (2007). Maca: An Andean crop Chemistry, 50, 666–679. with multi-pharmacological functions. Food Research International, 40, 783–792. León, J. (1964). The ‘‘Maca” (Lepidium meyenii), a little known food plant of Peru. Zhu, F. (2015a). Composition, structure, physicochemical properties, and Economic , 18, 122–127. modifications of cassava starch. Carbohydrate Polymers, 122, 456–480. Li, G. T., Wang, S. N., & Zhu, F. (2016). Physicochemical properties of starch. Zhu, F. (2015b). Isolation, composition, structure, properties, modifications, and Carbohydrate Polymers, 137, 328–338. uses of yam starch. Comprehensive Reviews in Food Science and Food Safety, 14, Li, J. Y., & Yeh, A. I. (2001). Relationships between thermal, rheological 357–386. characteristics and swelling power for various starches. Journal of Food Zhu, F., & Wang, S. N. (2014). Physicochemical properties, molecular structure, and Engineering, 50, 141–148. uses of sweetpotato starch. Trends in Food Science and Technology, 36, 68–78. Lindeboom, N., Chang, P. R., & Tyler, R. T. (2004). Analytical, biochemical and Zhu, F., Yang, X. S., Cai, Y. Z., Bertoft, E., & Corke, H. (2011). Physicochemical physicochemical aspects of starch granule size, with emphasis on small granule properties of sweetpotato starch. Starch/Stärke, 63, 249–259. starches: A review. Starch/Stärke, 56, 89–99. Zobel, H. F. (1988). Molecules to granules: A comprehensive starch review. Starch/ Lopez-Rubio, A., Flanagan, B. M., Gilbert, E. P., & Gidley, M. J. (2008). A novel Stärke, 40, 44–50. approach for calculating starch crystallinity and its correlation with double helix content: A combined XRD and NMR study. Biopolymers, 89, 761–768.