Introduction

Maize is a cereal with high commercial value and of global consumption; out of the 1060×10⁶t million tons produced, 40% is used for human consumption (FAOSTAT, 2013,2016). Consumption varies between regions and countries. As examples, the countries with the highest consumption volume in Africa are Lesotho, Malawi and Zambia, ranging from 325.15 to 433.97 g/person/day, while the countries with the highest consumption volume in the Americas are Mexico, Guatemala and Honduras, ranging from 213.60 to 318.74 g/person/day, and the countries with the highest consumption in Europe are Moldova, Bosnia-Herzegovina, and Romania, ranging from 110.88 to 251.42 g/person/day. This consumption suggests that the calorie consumption in carbohydrates, protein, minerals, and bioactive compounds from corn is also high and influences individual health.

Mexico is the center of origin, domestication, and diversification of maize, and it preserved a high diversity of colorations and characteristics of grain, precocity, plant and ear height, plant physiology, grain chemical composition, nutritional value and use (Kato et al., 2009; Vera-Guzmán et al., 2012;Fernández-Suárez et al., 2013). As a consequence, maize diversity is essentially distributed among indigenous communities or ethnolinguistic groups (Perales and Golicher, 2014). There is bias exists in maize research due to the importance of its trade, and most studies on corn grain composition focused on yellow and white grain; research on blue corn has only begun to focus in the last decade.

Pigmented grain maize contains phenolic compounds, carotenoid and anthocyanin, compounds associated with nutraceutical properties and health promotion benefits. Therefore, such grain is considered to be a functional food and features high antioxidant activities and preventive functions against cancer, diabetes, obesity and neurodegenerative disorders (Bañuelos-Pineda et al., 2018;Navarro et al., 2018). The most evaluated carotenoids in yellow maize are lutein, zeaxanthin, and α and β cryptoxanthin (Prasanthi et al., 2017), while the major anthocyanins in blue, red, and purple grains are cyanidin-3-glucoside (C3G), cyanidin-3,5-diglucoside, pelargonidin, and peonidin-3-glucoside and its malonyl derivatives (Aoki et al., 2002; Pedreschi and Cisneros-Zevallos, 2007; Guzmán-Gerónimo et al., 2017; Herrera-Sotero et al., 2017). Flavonoids are the least studied compounds and require more attention (Navarro et al., 2018).

Anthocyanin in maize grains is found in the aleurone layer, pericarp, or in both grain structures, and differ in concentration and structural distribution in the grain (González-Manzano et al., 2008; Espinosa-Trujillo et al., 2009; Salinas-Moreno et al., 2013). The genotype, environment, cultivation practices, genotype-environment interactions and pigment combinations in the grain influence the quantity and variety of anthocyanins or anthocyanidins (Giordano et al., 2018). Salinas-Moreno et al. (2012) evaluated different Mexican maize populations from the races Chalqueño and Bolite, and determined the anthocyanin contents to be 304.1 to 1332mg of C3G/kg of sample. Similarly, in populations of native maize from Colombia, Velásquez-Landino et al. (2016) reported values of 1.88 to 70mg C3G/100g and variations in total phenolic compounds of 538 to 1633mg gallic acid equivalents (GAE)/100g. Zilic et al. (2012) reported a content of total phenolic compounds of 5393.2mg·kg^-1 in yellow kernels. These results indicate that the genotype is relevant and interacts with the environment or cultivation practices. However, little has been documented in Mexican landraces, and this information is required to promote consumption and design conservation strategies that take advantage of this diversity.

In corn phenology, the filling phase and grain ripening are crucial for the synthesis of pigments and can be divided into four subphases. For example, yellow grains in the filling stage begin as a white-cream grain, then become yellow-cream, then yellow, and finally ripen to a yellow-golden or bright yellow. Xu et al. (2010) reported that moisture, sugar content, total phenolic compounds and carotenoids decrease, but the corncob subphase or yellow grain state showed the highest values of lutein, zeaxanthin and total carotenoids. A homologous event occurs with anthocyanin biosynthesis of the blue color in grain. These results indicate that some biotic and abiotic stress conditions in this phase influence the final bioactive compound content and may vary among genotypes due to the intrinsic variability in the time required by each genotype to complete this phase and how each genotype interacts with the growing environment. Kapcum and Uriyapongson (2018) reported that the temperature and storage time of blue-pigmented grain produced decreased anthocyanins (cyanidian-3-glucoside, pelargonidin-3-glucoside, and peonidin-3-glucoside) but showed no decrease in flavonoids or antioxidant activity, and consumption in postharvest days is recommended.

Biosynthesis, transport and/or accumulation of bioactive compounds such as anthocyanins, total phenolic and flavonoids in corn grain depend on multiple factors, such as environmental and cultivation practices, soil fertility, fertilizations, genotype, epigenetic factors and genotype-environment interactions (Harrigan et al., 2007;Jing et al., 2007; Khampas et al., 2015;Giordano et al., 2018). Other environmental factors affect the accumulation of anthocyanins, total phenolic compounds and antioxidant activity, including the amount and intensity of solar radiation, low temperatures and water stress (Chalker-Scott, 1999; Ali et al., 2010; Kishore et al., 2010). In this context, the objective of the present work was to evaluate the effects of cropping location, genotype (accession) and location-genotype interaction on the content of total phenolic compounds and antioxidant activities in a collection of pigmented native maize from Oaxaca, Mexico.

Materials and Methods

Collection and cultivation of germplasm

From December 2015 to March 2016, samples from 58 populations of yellow (30), red (13) and blue (15) native maize were collected in 39 municipalities of Valles Centrales, Sierra Norte, Sierra Sur, Mixteca and Papaloapan, Oaxaca, Mexico. During collection, the community, municipality, and region of origin, visual color of the grain, and the georeferenced locations of each community, from 278 to 2213masl, and within 17°59'59" to 16°30'37"W, and 98°19'69" to 96°00'30"N, were recorded. Three commercial varieties were added as controls: blue grain (VC-42 and SBA-4032) and yellow grain (Tuxpeño Basica). The collection and controls were planted in San Agustin Amatengo (July 5, 2016) and in Santa Maria Coyotepec (July 21, 2016), Oaxaca, under a randomized complete block design with four replicates. The traditional rainfed planting method was used at both locations, with irrigation support during grain filling to avoid water stress, and a fertilization formula of 120N-100P-60K was applied. Soil samples were extracted from the experimental locations for a general edaphic analysis using NOM-021-RECNAT (NOM, 2000) to describe the soil physicochemical properties (Table I).

Sampling and sample preparation for analysis

At harvest, a random sample of 10 healthy ears per accession or maize population was taken at each experimental location. The samples were manually threshed. A subsample of 100g of grain per population was then ground and crushed (Apex Construction^®, LTD and Krups^®, Mexico). The final flour was sieved through a 500μm mesh and stored in amber vials at -20°C until analysis.

Anthocyanin content in blue and red grain maize

The extraction of monomeric anthocyanins was performed from 3g flour samples with ethanol acidified at 85%. The monomeric anthocyanin content was determined by the differential pH method described by Wrolstad (1976). The absorbance of the reaction was measured with KCl pH 1 and CH₃COONa pH 4.5 in a spectrophotometer (Shimadzu UV-1800, Japan) at a wavelength range of 470-720nm, with measurements performed in triplicate. The monomeric anthocyanin (MA) concentration was calculated using the Wrolstad (1976) equation as follows: MA= (A×MW×DF×1000)/(ԑ×I), where A= (A510-A700) pH 1.0 - (A₅₁₀-A₇₀₀) pH 4.5, MW= 449.2g·mol-1 cyanidin-3-glucoside (C3G), ԑ= 26900 l·mol-1·cm-1 C3G molar extinction coefficient, DF= the dilution factor, and I= the cell length (1cm). The results are expressed as mg equivalent of C3G per 100g of dry sample (mg C3G/100g dw).

Total phenolic and flavonoid contents and antioxidant activities

The evaluation of the total phenolic and total flavonoid contents and the antioxidant activity was performed by extraction with 80% methanol from 3g of corn flour. The total phenolic content was determined by the method described by Singleton and Rossi (1965). We added deionized water and Folin-Ciocalteu reagent to 400μl of the diluted extract and left it to rest for 5min. Subsequently, 7% Na2CO3 was added, and the sample was incubated for 1h at room temperature (23 ±3ºC). Finally, absorbance readings were performed in triplicate in the spectrophotometer using distilled water as the blank. The total phenolic content was estimated as mg of gallic acid equivalent per 100g in dry basis (mg GAE/100g dw), compared with a calibration curve of gallic acid in concentrations from 0.02 to 0.125mg·ml^-1 (r²= 0.9982).

The flavonoid content was determined by the method of Zhishen et al. (1999). NaNO₂ 5% was added to the methanol extract, and it was stirred and left to rest for 5min. AlCl₃·6H₂O at 10% plus 1M NaOH and deionized water were then added. The absorbance was read in triplicate at 510nm and compared with a reactive blank. The flavonoid content was calculated as mg of catechin equivalent per g of dry sample (mg CE/g dw), based on a (+)-catechin calibration curve in concentrations from 0.0122 to 0.122µg·ml^-1 (r²= 0.9976).

The antioxidant activity of DPPH (2,2-diephenyl-1-picrylhydrazyl) was analyzed using the method of Brand-Williams et al. (1995). The DPPH radical was added to 100μl of the methanol extract. The solution was vortexed and allowed to stand for 30min in darkness. Subsequent readings were performed in triplicate at 517nm using a spectrophotometer and 80% methanol as a reference. Antioxidant activity was recorded based on a Trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid) calibration curve from 0.13 to 0.79μmol·ml^-1 (r²= 0.9984) and expressed in μmol Etrolox/g dw.

Antioxidant activity was also determined by the FRAP method. The antioxidant capacity, expressed as iron reduction, was determined by the method described by Benzie and Strain (1996). A total of 3ml of FRAP reagent (sodium acetate buffer pH 3.6, 10mM 2,4,6-tri(2-pyridyl)-s-triazine (TPTZ) and 10mM FeCl3 6H2O) were added to 100μl of the extract. This solution was incubated for 30min at 37°C. The absorbance was recorded at 593nm in the spectrophotometer. The quantification of antioxidant activity was performed based on a Trolox calibration curve from 100 to 1000μmol·l^-1 (r2= 0.9994), and the results are expressed as μmol equivalent of Trolox per g of dry weight (μmol ET/g dw).

Statistical analysis

To evaluate differences between cultivation locations, grain color groups, accessions nested in color groups, and location-color groups and location-accession interactions, analysis of variance was performed for each response variable based on the lineal model of combined analysis of randomized complete block design. Multiple means comparisons were performed using the Tukey method (p≤0.05). The location-accession interactions are represented in a graphical-descriptive manner, where each point represents the accessions as a function of the evaluation locations (= axes). All statistical analyses were performed using the SAS statistical package (SAS, 2000).

Results and Discussion

The anthocyanin content was evaluated in the red and blue grain maize populations. The analysis of variance detected significant differences (p<0.05) in anthocyanin content between locations, groups of color grains, accessions within groups, and locations-color groups and locations-accessions interactions. Regarding the total phenolic and flavonoid contents and the antioxidant activity (DPPH and FRAP), significant differences were found for all variables evaluated between grain color groups, cropping locations (except in flavonoids), accessions, and locations-groups and locations-accessions interactions. Notably, the anthocyanin content was evaluated only in samples of red and blue grains and, as previously reported, was absent in yellow grains where carotenoids were predominant (Espinosa et al., 2009;Zilic et al., 2012).

The cropping location influenced the average anthocyanin content in grain. In Santa Maria Coyotepec, blue and red maize had a significantly higher concentration of anthocyanins than San Agustin Amatengo. In addition, blue grain maize showed higher values than red grain maize. The significant interaction between the planting locations and grain color groups indicates that the blue grain group had higher anthocyanin concentrations in Santa Maria and San Agustin than red grain in both locations. Conversely, the lowest anthocyanins content was recorded in red maize cultivated in San Agustin. The significant interaction indicates that blue maize cultivation in Santa Maria had higher anthocyanin content and was favorably affected by the cultivation location (Table II). Therefore, the biosynthesis of secondary metabolites occurs via the synthesis of phenylalanine ammonia lyase, which is the enzyme responsible for catalyzing the transformation of L-phenylalanine to trans-cinnamic acid, and the enzymatic activity was influenced by environmental factors and water stress, high temperature, and incidence of UV radiation (Efeoğlu et al., 2009; Vogt, 2010;Chaves-Barrantes and Gutiérrez-Soto, 2017). Additionally, the synthesis of anthocyanins in maize occurs during the last grain-filling phase, and any environmental or physiological alteration in this phase influences the final anthocyanin content.

A high variation in the content of monomeric anthocyanins was identified between the red and blue grain accessions. The response patterns of the accessions follow the patterns observed previously in grain color groups. For example, in the group with the highest anthocyanin content, four accessions of blue grain and three of red grain with a content >30mg C3G equivalent in 100g dw were found. A variation between 22.7 and 29.5mg C3G/100g was observed in a group of 11 accessions of blue grain. Furthermore, three accessions of red corn varied between 20.7 and 25.2, five accessions exhibited values lower than 17.3, and practically no anthocyanins were detected in two accessions, with values <1mg C3G/100g. These results indicate that the visual coloration of faint or pale red was also indicative of low anthocyanin content in the grain, which was the case for accessions RJ01, RJ02, and RJ04 (Table III). On-farm, the preservation of blue, red, or yellow color in maize grain implies the planting of lots that require isolation in space or time, to avoid crossing and consequently the presence of different colors of grain in same cob. This independent management explains part of the difference in anthocyanin content between groups of red and blue grains.

The significant differences in anthocyanins among accessions or genotypes mean that the biosynthesis and storage capacity of anthocyanins in the grains differ from genotype to genotype, and the cropping location influenced these differences. Similar results were obtained by Salinas-Moreno et al. (2012) between races and maize populations of Chiapas, by Espinosa-Trujillo et al. (2009) in maize from central Mexico, by López-Martínez et al. (2009) in maize from different regions of Mexico, and by Guzmán-Gerónimo et al. (2017) in maize from the Oaxaca Mixteca region (21.4 to 66.9mg C3G/100g). These examples show that, despite the differences in laboratory protocols to obtain estimators of grain composition, the genetic diversity preserved in Mexico has been underutilized by rural communities and it not a priority in the maize breeding programs.

The interaction between cropping locations and groups of grain color affecting anthocyanin content distinguishes divergent patterns by grain color. For example, the red grains showed a downward and stable trend in both cropping locations. In contrast, ten accessions of blue grain exceeded the averages at both locations, over 25 and 22mg C3G/100g dw, in Santa Maria and San Agustin, respectively. As a function of the trend toward stability of anthocyanin content via cropping locations and in relation to the commercial variety (VC-42), two red and two blue grain samples stand out and surpassed the control. These four grains have a potential for continuous evaluations in other environments to demonstrate their stability across environments (Figure 1).

The content of total phenolic compounds, flavonoids and antioxidant activities in pigmented grains showed that the location and growing environment had significant effects on the concentration of the total phenolic content and antioxidant activity but not on flavonoids. In these assays, differentiation patterns among the grain color groups were in descending order of blue>red>yellow in content of total phenolic compounds, flavonoids, and antioxidant activities of DPPH and FRAP and were distinct (Table IV). Therefore, the higher content of bioactive compounds and antioxidant activity in the blue grain maize than in the other groups means that farmers exhibit independent management and seed selection in their lots of seeds as a function of grain color (Badstue et al., 2007), and these practices generated differences in the composition of total phenolic compounds, flavonoids and antioxidant activities.

The cropping locations had a significant effect on monomeric anthocyanin, total phenolic contents, and antioxidant activities (Tables IIand IV), and the Santa Maria location exhibited higher values than San Agustin. Location effects were considered climatic, and edaphic conditions grouped as an environmental effect. In this study, the Santa Maria location exhibited high values in soil electric conductivity (CE), organic matter, P, Mg, and Cu but a low pH compared to San Agustin Amatengo (Table I). These soil physical and chemical characteristics of Santa Maria favored the major absorption and mobilization of nutrients, biosynthesis of anthocyanins and phenolic compounds, and the high antioxidant activity, similar to the findings reported by Harrigan et al. (2007),Jing et al. (2007) and Khampas et al. (2015). For example, a pH close to 7.0 and sufficient organic matter in the soil enhance nutrient absorption (Farina et al. 1980).

A high variation in total phenolic content and flavonoids among the accessions allows the choice of the best accessions for direct utilization. The variation in total phenolic content ranged from 116.8 to 137.4mg GAE/100g in the blue grain accessions, from 93.2 to 166.4mg GAE/100g in red kernels and from 69.9 to 86.74 mg GAE/100g in yellow kernels. Flavonoids varied from 0.10 to 0.18mg CE/g in the blue grain accessions, from 0.08 to 0.19mg CE/g in red and from 0.02 to 0.05mg CE/g in yellow ones. The yellow grain accessions had the lowest contents of total phenolic compounds and flavonoids (Table V). These values are within the estimates of Salinas-Moreno et al. (2017) for the total phenolic content of maize accessions from different regions of Mexico, which ranged from 59.3 to 82.78mg GAE/100g, and for the values reported by Guzmán-Gerónimo et al. (2017) in Oaxacan Mixteca blue maize of 142.8 to 203.2mg GAE/100g. Our values surpass the values determined by Prasanthi et al. (2017) in different types of commercial maize in the USA, of 1.26 to 14.53mg GAE/100g. In all cases, high variability existed among the genotypes that can be used directly in food or to start a breeding program. However, the processing of the grain to its consumables (tortilla, cereal, totopo and other local foods) decreases the estimated contents of grain but retains up to 40% of the total (Herrera-Sotero et al., 2017; Prasanthi et al., 2017). These patterns are somewhat similar to the antioxidant activities of DPPH and FRAP as observed, for example, in the antioxidant activities evaluated by DPPH and FRAP in the accessions of blue grain. These results indicate that the accessions with higher total phenolic and total flavonoid content also have higher antioxidant activity.

Significant interactions between cropping locations and grain color groups were observed. In blue maize, a greater response was found in Santa Maria compared to San Agustin in the total phenolic compounds, flavonoids and antioxidant activities. A similar pattern of total phenolic and total flavonoid composition was also observed in red maize, and in particular, the antioxidant activity of DPPH in red grains was similar in both locations. The response for yellow maize was low with similar behavior in both cropping locations (Table VI). The agroecological conditions of the growing location affected the bioactive compounds and antioxidant activity of experimentally raised and developed grains.

For the cropping location-accessions interaction, only some accessions interacted with the environment in total phenolic and flavonoids content. Yellow grain accessions showed low phenolic and flavonoid contents at both growing locations. Conversely, some accessions of red grain strongly interacted with the cropping location (RJ10, RJ11, and RJ12), and others had high values (RJ01, RJ02, RJ04, and RJ06) and were stable. Blue grain accessions were stable from one location to another in phenol content but did not show a specific pattern in flavonoid content. Yellow grain and control accessions showed low flavonoid content. Two red grain accessions (RJ02 and RJ03) and two blue (AZ13 and AZ06) are remarkable, with flavonoid content >0.15mg CE/g (Figure 2). These data indicate that accessions of blue and red grains include a germplasm of high interest to initiate a process of maize breeding.

The antioxidant activity contributes to estimates of the potential of free radicals or the reducing capacities of the set of bioactive compounds stored in maize grains. Positive relationships between the composition of anthocyanins, total phenolic compounds, and flavonoids with their antioxidant activities were determined. Differences were observed between accessions, based on the antioxidant activities evaluated by DPPH together with FRAP. Nine blue grain and eight red grain accessions are noteworthy and showed higher antioxidant activity. For the total phenolic and total flavonoid contents, RJ02, RJ03, RJ04, RJ06, AZ10, AZ13, AZ16, and AZ18 stand out. Yellow grain accessions showed lower antioxidant activity and lower total phenolic and flavonoids levels (Figure 3). Relative to the FRAP-reducing capacity, the degree of hydroxylation and conjugation of phenolic compounds was confirmed (Pulido et al., 2000).

The evaluation of the interaction of locations and accessions revealed high variability and differential patterns among accessions in anthocyanin, total phenolic and flavonoid contents and antioxidant activities, which followed the patterns associated with the grain color group (Figures 1, 2 and 3). In bioactive compounds, the accessions of the blue grain always showed a pattern of higher content in Santa Maria and San Agustin, in contrast with the accessions of yellow grain, which showed low values, with the red grain falling between these two groups. In these cases, it possible to differentiate the accessions of blue and red corn with higher contents of anthocyanins, total phenolic compounds and flavonoids compared to yellow accessions, but their use in an integrated breeding program is possible in all cases. In terms of total phenolic compounds, some outstanding red accessions were RJ02, RJ03, RJ04 and RJ06, and some outstanding blue accessions were AZ10, AZ13, AZ16 and AZ18, among others.

Conclusions

The experimental results indicate that the environment and growing location affected anthocyanin and total phenolic content and antioxidant activity, and the effect differed as a function of the grain color group. The content of anthocyanin in blue grain maize was significantly higher compared to that of red grain maize. Among the groups of grain color, significant decreasing differences were determined as blue>red>yellow in total phenolic compounds, flavonoids, and antioxidant activities, and significant interactions between locations and grain color groups were observed. The highest values of anthocyanins, total phenolic compounds, flavonoids and antioxidant activities were found in Santa Maria Coyotepec. Additionally, a high variability between accessions was determined for all evaluated bioactive compounds and antioxidant activities, and significant interactions between locations and accessions of pigmented grains were observed. Some outstanding accessions in composition and antioxidant activity were RJ02, RJ03, RJ04, RJ06, AZ10, AZ13, AZ16 and AZ18, among others.

Acknowledgments

The authors are grateful for the financial support provided by CONACYT-Problemas Nacionales (Project no. 2015-1-1119) and the Instituto Politécnico Nacional (Project no. 20196672).

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Notas de autor

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