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Journal of soil science and plant nutrition

On-line version ISSN 0718-9516

J. Soil Sci. Plant Nutr. vol.13 no.1 Temuco Mar. 2013  Epub Feb 06, 2013

http://dx.doi.org/10.4067/S0718-95162013005000007 

Influence of genotype and harvest year on polyphenol content and antioxidant activity in murtilla (Ugni molinae Turcz) fruit

 

S. Alfaro1, A. Mutis2, R. Palma2, A. Quiroz2, I. Seguel3 and E. Scheuermann4,5*

1Programa de Doctorado en Ciencias de Recursos Naturales, Universidad de La Frontera, Casilla 54-D, Temuco, Chile. 2Laboratorio de Ecología Química, Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Casilla 54-D, Temuco, Chile. 3Instituto de Investigaciones Agropecuarias, INIA-Carillanca, Casilla 58-D, Temuco, Chile. 4Chemical Engineering Department, Universidad de La Frontera, Casilla 54-D, Temuco, Chile. 5Center of Food Biotechnology and Bioseparations, BIOREN-UFRO, Universidad de La Frontera, Casilla 54-D, Temuco, Chile. *Corresponding author: ericks@ufro.cl


Abstract

Polyphenol content and antioxidant activity in murtilla (Ugni molinae Turcz) fruit from three genotypes (the 14-4 genotype and the Red Pearl-INIA and South Pearl-INIA varieties) were studied over five growing seasons. Our results showed significant differences in total polyphenol content among yearly harvests. The lowest value (283 ± 72 mg GAE/100 g dw) was obtained for the 14-4 genotype in the 2008 harvest, and the highest value (2,152 ± 290 mg GAE/100 g dw) was observed for the variety South Pearl-INIA in 2007. The lowest value for antioxidant activity (2,234 ± 337 μmol TE/100 g dw) was obtained for the Red Pearl-INIA variety in 2008, and the highest value (4,073 ± 76 μmol TE/100 g dw) was observed for the 14-4 genotype in 2007. There was a significant effect of genotype and growing season on polyphenol content, antioxidant activity and dry matter content for the murtilla fruits evaluated in this study, but additional studies examining other abiotic and biotic factors are required to fully explain causality.

Keywords: DPPH, Trolox, rainfall, frost, climate conditions, native berry.


1. Introduction

The native Chilean species Ugni molinae Turcz, commonly called "murtilla," "mutilla" or "murta," is a wild perennial shrub that grows in southern Chile. This plant produces a small globoid berry with an equatorial diameter of 0.71-1.31 cm (Seguel et al., 2000). Infusions of murtilla leaves are highly valued in Chilean indigenous mapuche folk medicine for the treatment of conditions such as diarrhea, dysentery, and urinary tract pain (Montenegro, 2002). Murtilla is most often consumed as a fresh fruit because of its organoleptic characteristics, but the fruit is also processed commercially to be sold canned or as jam, juice or liquor (Scheuermann et al., 2008). Alfaro et al.

The murtilla fruit is known for its typical and surrounding aroma, which is produced by 24 volatile compounds that have been identified in four ecotypes and range in concentration from 1.2 to 250.5 μg kg-1 fresh weight (Scheuermann et al., 2008). Additionally, murtilla fruit is considered a valuable source of high quality pectin that has a chemical composition similar to that of commercial citrus pectin (Taboada et al., 2010). Several reports show an association between the antioxidant activity of murtilla fruits and leaves and the levels of polyphenols (Avello and Pastene, 2005; Rubilar et al., 2006; Shene et al, 2009; Ruiz et al., 2010; Rubilar et al., 2011).

Antioxidant activity studies using different ecotypes of murtilla have shown that the levels of antioxidant activity in the fruit are comparable to those of blueberry and lower than those of maqui and calafate fruits (Ruiz et al., 2010; Arancibia-Avila et al., 2011). These results suggest that high levels of flavan-3-ols such as catechin and epicatechin, in addition to the anthocyanins cyanidin-3-glucoside and peonidin-3-glucoside, could be the responsible for the high antioxidant activity observed in murtilla fruits. The concentration of flavonols observed in murtilla fruit was two times higher than the concentrations observed in maqui and calafate fruits, with quercetin derivatives being the most abundant flavonol (Ruiz et al., 2010).

Polyphenols and many other natural antioxidants (vitamins, carotenoids and other endogenous constituents) may promote better health. These antioxidants are capable of fulfilling a number of functional roles, acting as free radical scavengers, peroxide decomposers, singlet and triplet oxygen quenchers, enzyme inhibitors and synergists (Mandal et al., 2009). A close relationship has been shown between dietary intake of various antioxidant components and potential health benefits. However, several studies have found that these compounds may be affected by unaccounted factors, such as variety, growing environment, growing season, climate, temperature, light, soil type and other conditions (processing, post-harvest storage), which could affect both antioxidant content and antioxidant activity in the fruit (van der Sluis et al., 2001; Bolling et al, 2010).

The objective of this study was to determine potential seasonal differences in polyphenol content and antioxidant activity in murtilla fruits from three genotypes (the 14-4 genotype and the Red Pearl-INIA and South Pearl-INIA varieties) harvested in five different years.

2. Materials and methods

2.1. Sampling and experimental design

Fruits were obtained from three murtilla genotypes (the 14-4 genotype and the Red Pearl-INIA and South Pearl-INIA varieties) belonging to a germplasm collection developed by INIA-Chile through its murtilla research project. The plants were grown in an experimental field near Puerto Saavedra (38°45' S in latitude, 73°21' W in longitude). The genotypes used in this research were selected for their agronomical and organoleptic characteristics (Seguel et al, 2000; Scheuermann et al., 2008). The fruits were harvested in the same state and at the same stage in the plants' life cycle in April of 2006, 2007, 2008, 2009 and 2011 and were transported immediately after harvest to the Food Science Laboratory at the Universidad de La Frontera.

Total polyphenol content, antioxidant activity and dry matter of the murtilla fruit were determined for the three genotypes and the five harvest years (2006, 2007, 2008, 2009 and 2011). However, lack of financial support made it impossible to adequately manage the crops. Thus, the data from the fruit harvested in 2010 were excluded from the study due to low reliability.

2.2. Extraction

A solvent extraction of the murtilla fruit was used to measure polyphenol levels and antioxidant activity according to the methodology described by Scheuermann (2009). Approximately 6 g of fresh fruit was weighed with a semi-analytical balance (+/- 0.001 g) and ground with a mortar. The crushed fruit was subsequently transferred to a 100 mL bottle and 20 mL of methanol (99.9%) that had been previously conditioned to a temperature e of 30 °C was added. The solvent fruit extraction was performed in an oven (GFL-3032, Germany) under agitation (170 rpm) for 20 min at 30 °C. After the extraction step, the fruit extract was separated from solid matter by vacuum filtration using Advantec 232 filter paper (Toyo, Japan). The extracts were stored in 100mL flasks protected with aluminum foil and were analyzed immediately.

2.3. Total polyphenol content

Total polyphenol content was determined according to the method described by Wong et al. (2006). Using this method, 3.16 mL of distilled water were added to 40 μL of the sample and mixed with 200 μL of Folin-Ciocalteau reagent. After 5 minutes, 600 μL of 20% Na2CO3 were added to the reaction mixture and the mixture was allowed to stand for 120 min. The absorbance of each sample was measured at 765 nm and expressed in mg of gallic acid equivalents (GAE) per 100 g of dry weight (dw) by calibrating the optical density of each sample to a standard curve that was previously established using varying concentrations of gallic acid.

2.4. DPPH antioxidant activity

The antioxidant capacity of the murtilla fruit extracts was determined by measuring the radical 2,2-diphenyl-1-picrylhydrazy (DPPH) scavenging of the antioxidant compounds present in the extracts. The degree of discoloration of the solution indicated the scavenging efficiency of the added substance. In its radical form, DPPH has an absorption band of 515 nm, which disappears following reduction by an antiradical compound (von Gadow et al., 1997; Atoui et al., 2005). The initial absorbance of the DPPH in methanol was measured at 515 nm and had a range of 0.630 to 0.640. An aliquot (50 μL) of the murtilla fruit extract was added to 1,950 μL of the metanolic DPPH solution. The change in absorbance at 515 nm was measured at 30 min. The antioxidant capacity, based on the DPPH free radical scavenging ability of the extract, was expressed in μmol Trolox equivalents (TE) per 100 g of dry weight (dw).

2.5. Dry matter

Dry matter was determined using fruit moisture content according to the Instituto de Salud Pública de Chile (1998). Five grams of halved murtilla fruits were oven-dried at 105 °C for five hours and then weighed. This process was repeated until the difference between two successive weighings was less than 5 mg.

2.6. Climate condition data

Climate records for rainfall and number of frosts were obtained from the closest meteorological station, located in Tranapuente (38°41' S, 73°21' W). The first growing season (2006) ran from May 2005 to April 2006 when the fruit was harvested. The growing season was the same during subsequent years, up through the final harvest in April 2011.

2.7. Data analysis

For all experiments, three to five replicates were analyzed per treatment. The data were analyzed using a mixed-model ANOVA with genotype and season, followed by Tukey's Honestly Significant Difference tests as pos-hoc tests (Sokal and Rohlf, 1995). Alternatively, Student's t-tests were used to analyze pairs of independent samples (Zar, 1999). Prior to performing the statistical tests, the data for each variable were checked for normality and homogeneity of variance. A canonical discriminant analysis was performed to evaluate murtilla genotype performance using 95% confidence ellipses. Total polyphenol content, antioxidant activity and dry matter were correlated with rainfall and number of frosts (measured in the field) using the nonparametric Spearman's rank method. JMP v.8 software (SAS Institute Inc., Cary, NC) was used for all statistical analyses and differences were considered significant at p< 0.05.

3. Results and Discussion

3.1. Total polyphenol content, DPPH antioxidant activity and dry matter of murtilla fruit from different growing seasons

The effect of harvest year on total polyphenol content, DPPH antioxidant activity and dry matter for the three genotypes studied was significant (Tukey's test, p<0.05) (Figure 1). Large differences in total polyphenol content were observed among harvest years, with polyphenol content ranging from 283 ± 72 mg GAE/100 g dw for the 14-4 genotype in 2008 to 2,152 ± 290 mg GAE/100 g dw for the South Pearl-INIA variety in 2007. DPPH antioxidant activity ranged from 2,234 ± 337 μπω! TE/100 g dw in the Red Pearl-INIA variety in 2008 to 4,073 ± 76 μmol TE/100 g dw for the 14-4 genotype in 2007.

Figure 1. Total polyphenol content (mg GAE/100 g dry weight), DPPH antioxidant capacity (μπκ)ΠΈ/100 g dry weight) and dry matter (%) in murtilla fruit for the genotype and the two varieties over the five study years.
14-4 G: Genotype 14-4; RP-I: Red Pearl-INIA variety; SP-I: South Pearl-INIA variety. f Missed treatment. Letters for each combination of parameter/year indicate significant differences according to the HSD-Tukey test (Student's t-test was used to compare treatments within the 2006 harvest year) (p<0.05).

These differences could be explained by variation in weather conditions among the growing seasons, such as differences in rainfall and the number of frosts. The highest correlations were between total polyphenol content and rainfall, dry matter and rainfall, dry matter and number of frosts and DPPH antioxidant activity and rainfall (Table 1). These abiotic factors could also be responsible for the changes in dry matter. For instance, notable changes in fruit dry matter between the 2006 and 2009 harvest years were observed for the 14-4 genotype (30.9% decrease) and the Red Pearl-INIA variety (33.2% decrease) (Figure 1). This result is corroborated by the significant correlations between dry matter and rainfall (0.82) and dry matter and number of frosts (0.75).

Table 1. Precipitation and number of frosts by growing season and their degree of correlation with the parameters measured in murtilla fruit.
a Missing data. b. All correlation coefficients (Spearman's rho) are significant at the p<0.001 level. Numbers in parentheses indicate sample size. DPPH AA: DPPH antioxidant activity.

Therefore, our results showed a trend in increasing total polyphenol content, DPPH antioxidant activity and dry matter with increasing rainfall and number of frosts. Several researchers attribute differences in the level of phenolic compounds and antioxidant activity in fruits and vegetables of the same genotype grown in different locations or different years to changes in environmental conditions, such temperature, water availability (drought or precipitation), light intensity, salinity and pollination (van der Sluis et al, 2001; Connor et al, 2002; Howard et al., 2003; Temime et al., 2006; Ksouri et al., 2008; Bolling et al., 2010; Kevers et al., 2011; Sun et al., 2011). However, the mechanism behind the effects of low temperature (number of frosts) and water availability (rainfall) on phenolic content and other secondary metabolites in plants is not clearly understood. Normally, the mechanism considered the biotic or abiotic stresses that result in the formation of reactive oxygen species (ROS) followed by activation of the enzyme and hormone systems of the plant, producing antioxidants that include enzymatic and non-enzymatic components (Xin and Browse, 2000; Janda et al., 2003; Ksouri et al., 2008). The effects of water stress (e.g., waterlogging or drought) and temperature (low v. high, constant v. fluctuating) on the medicinal herb Hypericum brasiliense included an increase in the levels of some phenolic compounds (quercetin, rutin, 1,5-dihydroxyxanthone and isouliginosin B). However, changes in phenolic content depended on the type of stress and the compound analyzed and were likely a response to the generation of ROS (de Abreu and Mazzafera, 2005).

Figure 2 shows the values for monthly total rainfall and minimum accumulated temperature used to correlate each growing season (Table 1) with total polyphenol content, DPPH antioxidant activity and dry matter for the three murtilla fruit genotypes. As shown in Figure 2A, the accumulated rainfall values for the month of August in the 2005-2006 and 2010-2011 growing seasons were similar to the total rainfall in the 2007-2008 and 2008-2009 growing seasons.

Figure 2. Changes in monthly total rainfall (A) and minimum accumulated temperature (B) for each growing season. Correlations with total polyphenol content, DPPH antioxidant activity and dry matter of the three murtilla fruit genotypes (the 14-4 genotype and the Red Pearl-INIA and South Pearl-INIA varieties) are shown in Table 1.

There were differences in rainfall distribution and quantitative rainfall between April 2005 and April 2011, confirming that there was variance in this agronomic parameter over the course of the study period at the location of the experimental field is located (38°45' S latitude; 73°21'W longitude). A similar pattern occurred for minimum accumulated temperature (Figure 2B), with the 2008-2009 growing seasons showing the highest temperature (44 °C) and the lowest the number of frosts (Table 1) for the study period.

Year-to-year variations in certain phenolic compounds that are important sources of secondary plant metabolites have been observed in other types of fruit (van der Sluis et al., 2001; Kevers et al., 2011). Connor et al. (2002) reported that the phenolic content of several highbush and interspecific hybrid blueberry cultivars grown at three locations varied considerably over two growing seasons. Howard et al. (2003) suggested that this effect was not surprising because abiotic and biotic factors such as temperature, irradiation, herbivory and pathogenic infection are known to induce the protective antioxidant mechanisms of plants. The correlation coefficients determined by Sun et al. (2011) showed that altitude and annual precipitation had a significant effect on sour jujube fruit (Ziziphus jujuba Mill.). Fruits grown in harsh, arid and high-altitude areas can produce a larger amount of natural antioxidants and therefore may exhibit higher antioxidant activities than fruits grown in other areas.

3.2. Genotypic and seasonal effects on total polyphenol content, DPPH antioxidant activity and dry matter of murtillafruit

The analysis of variance showed that the effects of genotype, season and genotype x season were significant for all variables, with the exception of genotype and genotype x season for DPPH antioxidant activity (Table 2).

Table 2. F-values and significance of the main effects and interaction effect of the variables analyzed by multifactorial ANOVA.

* p<0.05; ** p<0.01

ns: non-significant difference.

Howard et al. (2003) reported similar results in blueberries and attributed these results to genetic and environmental factors. The significant main effects of growing season, genotype and genotype x growing season on antioxidant activity measure by the Oxygen Radical Absorbance Capacity (ORAC) test, phenolic content and fruit weight demonstrated that environmental growing conditions can impact phenolic and ORAC levels in blueberry and that genotypes vary in their capacity to synthesize phenolic compounds under different growing conditions. In contrast, Connor et al. (2002) found that the antioxidant activity and phenolic content of blueberry cultivars were more strongly affected by genotype than by harvest year.

Correlation does not imply causation, but a correlation does indicate that changes in one variable are related to changes in another variable. New studies that include other abiotic and biotic factors are necessary to determinate all of the causes that could fully explain year-to-year changes in total polyphenol content, DPPH antioxidant activity and dry matter in the murtilla fruit varieties evaluated in this study. It is the first whose purpose is to relate some environmental and chemical variables for this fruit.

3.3. Importance of genotype

The multivariate discriminant analysis of murtilla genotypes resulted in two canonical variables accounting for 94.2% and 5.7% of the variation between genotypes. Reduced space plots of the two canonical variables distinguished among the genotypes based on 95% confidence ellipses (Figure 3). The analysis showed that the responses of the Red Pearl-INIA variety (RP-I) and the 14-4 genotype (144G) were indistinguishable from each other under the conditions of this study, while the South Pearl-INIA (SP-I) variety appeared to have a significantly different effect.

Figure 3. Canonical discriminant analysis of murtilla varieties based on polyphenol content, DPPH antioxidant activity and dry matter. Labels: SP-I: South Pearl-INIA variety, RP-I: Red Pearl-INIA variety, 14-4G: 14-4 genotype. Data represent the first and second canonical variables (Canonical 1 and Canonical 2) for the murtilla sample by variety (95% confidence ellipses).

In this study we demonstrated the effect of genotype and growing season on total polyphenol content, DPPH antioxidant activity and dry matter in murtilla fruit. There are reports showing that antioxidant activity in the fruits and leaves of blackberry, raspberry, and strawberry plants varies with cultivar and developmental stage (Wang and Lin, 2000). In one study, apple polyphenol content varied by at least 5.2-fold among 67 cultivars (Wojdylo et al., 2008). The effect of genotype on antioxidant activity has been shown in grapes (Lee and Talcott, 2004), plums (Gil et al., 2002), apples (Wolfe et al., 2003), citrus fruits (Bocco et al., 1998), guavas (Jiménez-Escrig et al., 2001), nectarines and peaches (Gil et al., 2002). Bolling et al. (2010) found seasonal differences in total phenol and antioxidant constituents in almonds, reporting a 13% greater polyphenol content between different cultivars in 2005 compared to 2007. Because the qualitative and quantitative composition of phenolic compounds in fruits is unique to individual species and genotypes, it is possible to determine similarities and differences among standardized and confirmed genotypes and predict the response of new varieties to specific production and cultivation conditions (Sochor et al., 2010).

In this study, high correlations were found between climatic factors (rainfall and number of frosts) and the fruit characteristics evaluated (Table 1). Similar results were observed by Temime et al. (2006), who reported a positive linear relationship between precipitation and phenol content in Chétoui variety virgin olive oils. Moreover, the results of Janda et al. (2003) suggest that plants grown at low temperatures have higher levels of both antioxidants and antioxidant enzymes, and Xin and Browse (2000) suggest that low temperatures induce changes in plants, such as increased levels of antioxidants and reduced water content.

 

4. Conclusions

In summary, in this study, there was a statistically significant effect of growing season on polyphenol content, antioxidant activity and dry matter of murtilla fruits from three genotypes (the 14-4 genotype and the Red Pearl-INIA and South Pearl-INIA varieties). These characteristics trend to increase with higher rainfall and number of frosts. In addition, polyphenol content and dry matter were affected by genotype. A canonical discriminant analysis of seasonal differences in the Red Pearl-INIA, South Pearl-INIA and 14-4 genotypes showed that the South Pearl-INIA variety varied the most from the other genotypes. Additional studies that examine other biotic and abiotic factors that affect secondary metabolites are needed to fully explain the causes of year-to-year variation in polyphenolic compounds and antioxidant activity in murtilla fruit.

Acknowledgements

The authors are grateful for the financial support provided by Project DIUFRO 120622 of the Universidad de La Frontera and Project FONDEF D05I10086 of the Instituto de Investigaciones Agropecuarias INIA-Carillanca, the Universidad de La Frontera and the Universidad Austral de Chile.

 

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