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Crop Science 41:1676-1681 (2001)
© 2001 Crop Science Society of America

CROP BREEDING, GENETICS & CYTOLOGY

Antioxidant Activity and Phenolic Content of Oat as Affected by Cultivar and Location

Cheryld L. Emmonsa and David M. Peterson*,b

a Division of Biology, Alfred University, Alfred, NY 14802
b USDA-ARS Cereal Crops Research Unit, 501 Walnut Street, Madison, WI 53705 and Department of Agronomy, University of Wisconsin-Madison

* Corresponding author (dmpeter4{at}facstaff.wisc.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 NOTES
 RESULTS AND DISCUSSION
 REFERENCES
 
Phenolic compounds in oat (Avena sativa L.) may have health-promoting effects on humans due to their antioxidant or other properties. The objective of this study was to determine the effects of cultivar and location on phenolic contents and antioxidant activities of alcohol-soluble extracts from oat groats. Antioxidant activities (AOA) and concentrations of eight phenolic compounds having AOA were measured in three cultivars grown at seven locations in Wisconsin during 1998. There were significant differences among cultivars for AOA, concentrations of all of the phenolic compounds measured except p-coumaric and ferulic acids, and for total free phenolic contents (FPC). Location significantly affected the concentrations of five of the phenolics and total FPC, but did not affect AOA. There were significant cultivar x location interactions for the concentrations of avenanthramides and for total FPC. The unexpectedly high concentrations of avenanthramides from the Sturgeon Bay location were confirmed by analysis of groats from 1999 and 2000. It should be possible to improve the AOA and phenolic concentrations of oat as quantitative traits in a cultivar development program, but significant location effects may attenuate rapid progress.

Abbreviations: AOA, antioxidant activity • ARL, Arlington • ASH, Ashland • AVA [or B, or C], avenanthramide A [or B, or C] • BHT, butylated hydroxytoluene • CA, caffeic acid • CHI, Chilton • FA, ferulic acid • FD, ferulate derivative • FPC, free phenolic contents • GA, gallic acid • HPLC, high-performance liquid chromatography • MAD, Madison • MAR, Marshfield • PCA, p-coumaric acid • SBY, Sturgeon Bay • SPO, Spooner • VAN, vanillin


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 NOTES
 RESULTS AND DISCUSSION
 REFERENCES
 
NATURALLY OCCURRING PLANT PHENOLICS include several groups of compounds that have potential health-promoting properties. Phenolics may act as antioxidants, thereby reducing the risk of atherosclerosis and coronary heart disease, which can be caused by oxidation of low-density lipoproteins (Gey et al., 1991; Ulbricht and Southgate, 1991; Castelluccio et al., 1995). They also may protect against some forms of cancer (Clifford et al., 1996). Oat phenolics with AOA include simple phenolics, such as ferulic acid (FA), caffeic acid (CA), p-coumaric acid (PCA), and vanillin (VAN), in free and bound forms, and flavonoids such as kaempferol and quercetin (Daniels et al., 1963; Daniels and Martin, 1967; Durkee and Thivierge, 1977; Collins, 1986; Duve and White, 1991; Dimberg et al., 1996; Xing and White, 1997). A group of phenolic compounds with AOA that is unique to oat is the avenanthramides, N-cinnamoyl derivatives of anthranilic acid (Collins, 1986, 1989; Dimberg et al., 1993).

Phenolic contents of oat have been reported from several laboratories, but only one report compares the variation in contents among different oat cultivars. Dimberg et al. (1996) compared three Swedish cultivars and found them to differ significantly in FA, CA, PCA, VAN, and avenanthramide contents. Concentration ranges of three of the avenanthramides were 21 to 62 mg kg-1, which were 10- to 30-fold greater than those of the simple phenolics (FA, CA, PCA, and VAN), which ranged from about 1.3 to 2.7 mg kg-1. No information is available concerning environmental effects on phenolic contents of oat. Genetic and environmental effects on AOA of oat extracts have not been reported in the literature. The concentrations of tocols, which are known to have AOA, were significantly affected by genotype and location (Peterson and Qureshi 1993). The objective of this study was to evaluate the relative importance of cultivars, locations, and their interaction on phenolic contents and AOA of alcoholic extracts of oat by testing three cultivars grown at seven locations in replicated plots.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
NOTES
 RESULTS AND DISCUSSION
 REFERENCES
 
Grain samples of oat cultivars Belle, Dane, and Gem were obtained from seven locations in Wisconsin, USA, as part of varietal trials conducted by the University of Wisconsin oat breeding project in 1998. In a followup study, grain samples of the same cultivars from two of the locations from the 1999 and 2000 growing seasons were analyzed. Dane, Belle, and Gem are early, mid-season, and late maturing spring cultivars, respectively, adapted to the midwestern USA (Duerst et al., 1999; Forsberg et al., 1999; Oplinger et al., 1999). Gem and Belle are resistant to crown rust (Puccinia coronata Corda var. avenae W.P. Fraser & Ledingham), whereas Dane is susceptible. At each location these cultivars, among others, were arranged in a randomized complete block design. Plots varied in size among locations from four to ten rows, either 3 or 12 m in length. Seeding rate was 3200 to 3500 seeds m-2. In 1998, there were two blocks at Arlington (ARL) and Marshfield (MAR) and four at Ashland (ASH), Chilton (CHI), Madison (MAD), Spooner (SPO), and Sturgeon Bay (SBY). In 1999, there were two blocks from ARL and SBY, and in 2000, two blocks from ARL and four from SBY. From each plot 2.4-m sections of two center rows were mechanically harvested and threshed. The soil types were as follows: ARL and MAD, Plano silt loam; fine-silty, mixed, superactive, mesic Typic Argiudolls; ASH, Portwing silt loam; fine, mixed, superactive, frigid Oxyaquic Glossudalfs; MAR, Withee silt loam; fine-loamy, mixed, superactive, frigid Aquic Glossudalfs; SBY, Longrie silt loam; coarse-loamy, mixed, frigid Entic Haplorthods; SPO, Antigo silt loam; coarse-loamy over sandy or sandy-skeletal, mixed, superactive, frigid Haplic Glossudalfs. The plots at CHI were on a private farm on a red clay. Soil maps are unavailable for this area. The ARL and MAD sites are in southern Wisconsin, CHI, MAR, and SBY are mid state, and ASH and SPO are in northern Wisconsin. Crown rust disease ratings, from 0 to 100, were made for each cultivar at ARL and MAD by Ron Duerst, University of Wisconsin, Department of Agronomy. Rainfall conditions in 1998 were normal except for a dry July. Harvest conditions were good, disease problems were few, and grain yields were within normal expectations.

Samples from each plot were separated into hulls and groats using an impact dehuller. Duplicate 5-g subsamples of groats were ground to pass through a 0.5-mm screen (Brinkman ZM-1 mill, Westbury, NY).1 One gram of each subsample was extracted with 13.7 mol L-1 (80% v/v) ethanol (3 x 10 mL) with shaking for 20 min. The first extraction was at 50°C and subsequent extractions were at room temperature. Extracts were centrifuged (1250 g for 5 min) and the supernatants collected, combined, and dried in vacuo at 40°C. Residues containing the extracted phenolics were dissolved in 2 mL of methanol, filtered through a 0.2-µm polyvinylidene difluoride (PVDF) membrane, and stored at -20°C until analyzed. Antioxidant activity was measured within 48 h of extraction. Component separation by high-performance liquid chromatography (HPLC) was completed within 2 wk of extraction. Preliminary tests showed that the extracts were stable at this temperature for 2 wk.

Antioxidant activity was measured as the inhibition of the coupled autoxidation of linoleic acid and ß-carotene as compared with a control (Marco, 1968; Miller, 1971; Lee et al., 1995). Extracts were diluted with methanol to the equivalent of 2 mg starting material per 40 µL. ß-Carotene (2 mg) was dissolved in 40 mL of chloroform, and 6 mL of this solution was combined with linoleic acid (40 mg) and Tween 40 (400 mg). The mixture was divided into 1.5-mL aliquots and the chloroform was removed under a stream of N2 gas. Oxygenated deionized water (25 mL, 50°C) was added and mixed well. Aliquots (3 mL) of the ß-carotene–linoleic acid emulsion were mixed with 40 µL of each sample. Oxidation of the emulsion was monitored spectrophotometrically by measuring absorbance at 470 nm at 30-s intervals for 15 min at 50°C (Shimadzu UV-2101 PC scanning spectrophotometer with a temperature controlled 6-cell CPS-260 cell positioner, Shimadzu Scientific, Columbia, MO). Controls contained 40 µL of methanol in place of the extract. Antioxidant activity was expressed as the percentage of inhibition of ß-carotene bleaching relative to the control for the time interval between 5 and 15 min, during which time the rate was linear, using the equation:

[1]
where AOA is antioxidant activity, DRc is the degradation rate of control, and DRs is the degradation rate of a sample (Al-Saikhan et al., 1995). Degradation rates were computed by regression analysis.

Phenolic compounds were separated by reversed-phase HPLC. Samples (20 µL) were injected onto a C18 reversed-phase column (µBondapak, 250 by 4.6 mm, 10-µm particle size, Waters, Milford, MA) and eluted over 75 min with a linear gradient of 1 to 40% HPLC-grade acetonitrile in water adjusted to pH 2.8 with acetic acid, or for measuring avenanthramides only, a 25 to 55% acetonitrile gradient over 18 min was used. The flow rate was 1 mL min-1 and the eluate was monitored at 290 nm for the simple phenolics and 330 nm for the avenanthramides. Peaks were identified by comparing retention times and UV scans (200–360 nm), using a diode array detector (model SD-M10VP, Shimadzu Scientific), with known authentic standards. Peak identities were further verified by coelution with internal standards. Quantitation was achieved by comparing peak areas with external standards (CA, FA, PCA, and VAN from Sigma-Aldrich, St. Louis, MO; avenanthramides A, B, and C (AVA, AVB, and AVC) were synthesized following the methods of Collins (1989) and confirmed by nuclear magnetic resonance). A tentatively identified ferulate derivative (FD) was quantified as FA equivalents (mg kg-1).

The concentration of total free (alcohol soluble) phenolics (FPC), measured as gallic acid (GA) equivalents, was determined using the Folin & Ciocalteau's phenol reagent (Ragazzi and Veronese, 1973). One milliliter of a sample (diluted to 50% of original concentration with methanol), 0.5 mL of phenol reagent (Sigma-Aldrich), and 3.0 mL of Na2CO3 (200 g L-1) were combined in the given order. The mixture was vortexed and the reaction allowed to proceed for 15 min at room temperature. All samples were diluted with 10 mL of deionized water. A white precipitate that formed from the phenol reagent was removed by centrifugation (5 min at 1250 g). Absorbance of the supernatants was measured at 725 nm. Methanol was used as a blank in place of the sample. Gallic acid equivalents (mg kg-1) were determined from a GA standard concentration curve.

The data from each location were analyzed separately by analysis of variance. A combined analysis of variance for all locations as a split-plot design was performed. Genotype, location, and genotype x location effects were determined using blocks as replicates with measures from duplicate extractions for each plot. The analysis of variance was performed with the general linear model (GLM) of the SAS software package (release 7.0) (SAS Institute, 1998) analyzing cultivar and location as fixed effects. Homogeneity of variances among locations was tested using Levene's test, and followed by Welch's ANOVA (SAS Institute, 1998). Means separation was by least-squares analysis. Regression analyses were performed with the PROC REG procedure of the SAS software package.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 NOTES
 RESULTS AND DISCUSSION
REFERENCES
 
We found significant differences among the three cultivars for AOA, all of the phenolics except PCA, and total free phenolic content (Table 1). Differences among locations were significant for CA, PCA, the avenanthramides, and total free phenolic content. There were significant cultivar x location interactions for PCA and the avenanthramide concentrations and total free phenolic content.


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  		Table 1. Analysis of variance mean squares and significance for cultivar, location, and cultivar x location interaction effects for antioxidant activity and phenolic contents of three oat cultivars grown at seven locations.

 
Cultivar Effects
Dane and Belle had the highest AOA, followed by Gem (Table 2). These differences were significant for data combined across all locations, but significant only for the MAR location when analyzed on a by-location basis. At every location, Gem had the lowest activity, and the activity for Dane was greater than or equal to that for Belle. Dane and Gem have closely related pedigrees that include ‘Ogle’ as a male parent and breeding line X3530-47 as a parent or grandparent (Duerst et al., 1999 and Ron Duerst, Univ. of Wisconsin-Madison, 1999, personal communication). The finding that these two closely related cultivars differ in their antioxidant activities suggests that a small number of genes control AOA, and screening of a more diverse population would identify genotypes with a wider range of antioxidant activities.


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  		Table 2. Antioxidant activity and phenolic concentrations of three oat cultivars.{dagger}

 
Mean CA concentrations ranged from 0.23 to 0.41 mg kg-1 among cultivars, and they were significantly higher in Belle and Dane than in Gem (Table 2). Dane had higher CA concentrations at five of the seven locations. This high CA concentration may account for Dane having the highest AOA, even though it had lower levels of other antioxidant components. Caffeic acid has been reported to have a higher AOA than other simple phenolics (Castelluccio et al., 1995; Chen and Ho, 1997; von Gadow et al., 1997; Milic et al., 1998; Pannala et al., 1998; Vieira et al., 1998). Caffeic acid concentrations of three Swedish oat cultivars were 5- to 10-fold higher (Dimberg et al., 1996) than those reported here. Vanillin concentrations ranged from 1.33 to 2.29 mg kg-1, the highest level being in Belle. This range was slightly lower than the one reported by Dimberg et al. (1996) (2.1–2.6 mg kg-1). Belle was lower than the other cultivars in FA concentration. As compared with a previous analysis of different samples of these same cultivars, CA concentrations were lower, VAN and FA higher, and PCA similar to those found previously (Emmons and Peterson, 1999). Gem had significantly higher levels of FD than Belle or Dane.

There are several putative avenanthramide peaks that appear on the chromatograms, but typically three peaks are much higher than the others, and we have identified these as avenanthramide A, B, and C (Collins, 1989). Avenanthramide concentrations were much higher than concentrations of the simple phenolics in all three cultivars (Table 2). The mean concentrations across locations of each of the measured avenanthramides were higher in Belle and Gem than in Dane. Avenanthramide C was highest in concentration among the three avenanthramides measured for each cultivar. Dimberg et al. (1993) reported a higher range (40–132 mg kg-1) for AV1 (AVB) concentration among 12 cultivars. In a subsequent study (Dimberg et al., 1996), they reported values for avenanthramide concentrations that were very similar to our findings.

Avenanthramides are synthesized in leaf tissue in response to attack by incompatible races of the pathogen, Puccinia coronata Corda, the causal agent of crown rust (Mayama et al., 1982; Miyagawa et al., 1995). Belle and Gem are resistant to crown rust (Duerst et al., 1999; Forsberg et al., 1999) and showed negligible disease in the field at ARL and MAD (disease ratings of 0 to 1) as compared with Dane, which is susceptible (disease ratings of 35 to 40). We did not sample leaf tissue for analysis. Avenanthramides are present in grain tissue regardless of whether the plant is under fungal attack. The lower concentrations in susceptible Dane as compared with resistant Belle and Gem may indicate an association with crown rust resistance, but this hypothesis has not been tested.

Differences in total FPC among cultivars (Belle > Gem > Dane) were similar to cultivar differences in the avenanthramides concentrations (Table 2). This was expected because the avenanthramides comprise the majority of the phenolic substances present in oat extracts.

Location Effects
Levene's test indicated that variances among locations were not homogeneous for the avenanthramides and total free phenolic content, but Welch's ANOVA showed that there were significant differences among location means. There were significant differences among locations for concentrations of five of the eight phenolic compounds quantified and for FPC (Table 1). The CA concentration at ARL was significantly lower than that at all other locations (Table 3). p-Coumaric acid concentration was significantly higher at SBY than the other locations. Ferulic acid, FD, and VAN concentrations were not significantly different among locations. The AVA, AVB, and AVC concentrations were more than twofold greater at SBY than at any other location. Free phenolic contents was also highest at SBY, followed by MAD (Table 3).


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  		Table 3. Mean antioxidant activity and phenolic concentrations of oat grown at seven locations.{dagger}

 
Because of the extreme difference in levels of avenanthramides between SBY and the other locations, seed from the 1999 and 2000 crop years at SBY and ARL was obtained and analyzed for avenanthramide concentrations. The data were consistent for all 3 yr: SBY was significantly higher than ARL, although the margin of difference was less in 2000 (Fig. 1) . This followup experiment also confirmed the lower levels of avenanthramides in Dane compared with Gem and Belle.



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  		Fig. 1. Concentrations of the avenanthramides A, B, and C (AVA, AVB, and AVC) for three oat cultivars grown at Arlington (ARL) and Sturgeon Bay (SBY) in 1998, 1999, and 2000. (A) Mean values for each cultivar across locations. In each year, the concentrations of avenanthramides were significantly greater in Belle than Gem, and in Gem than Dane (P = 0.05) except for AVA in 1998 and AVC in 2000, where Belle and Gem were not different. (B) Mean value for each location across cultivars. In each year, the concentrations of avenanthramides were significantly (P = 0.05) greater from SBY than ARL.

 
Interaction Effects
Cultivar x location interaction effects for PCA, the avenanthramides, and total free phenolic content were significant (Table 1). The significant interaction for CA resulted from higher concentrations in Belle at CHI and SPO, but higher in Dane at the other locations. The cultivar–location means for avenanthramides and FPC are plotted in Fig. 2 . Madison was the second highest location for avenanthramide and total free phenolic concentrations for Belle and Gem, but for Dane, concentrations were low at MAD compared to other locations (Fig. 2). From the analysis of data for each location separately, it was shown that cultivars did not differ significantly in AVA concentration for the ARL and SPO locations, but differed for the other locations. The AVB concentrations did not differ significantly among cultivars for the ARL and ASH locations, but did show differences for all other locations. Cultivars did not differ in AVC concentrations for the ARL, ASH, and SPO locations, but did at SBY, MAD, CHI, and MAR. Total free phenolic content differed among cultivars for the MAD, MAR, and SBY locations, but not for the other four locations.



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  		Fig. 2. Concentrations of the avenanthramides and total free phenolic contents for three oat cultivars grown at seven locations in Wisconsin in 1998. (A) avenanthramide A (AVA); (B) avenanthramide B (AVB); (C) avenanthramide C (AVC); (D) free phenolic contents (FPC). Locations were Ashland (ASH), Arlington (ARL), Chilton (CHI), Marshfield (MAR), Spooner (SPO), Madison (MAD), and Sturgeon Bay (SBY).

 
Cultivar and/or location effects influenced the total free phenolic content and concentrations of each phenolic identified, except FA. Cultivar effects were greater, as determined by comparing the magnitude of the mean squares and their proportions in relationship to total variability (total mean squares), than location effects for AOA, VAN, and FD, whereas location effects were greater than cultivar effects for PCA, the avenanthramides, and total free phenolic content (Table 1). The cause of location effects has not been identified, but appears to be primarily due to characteristics of the ARL location (for CA and VAN) and SBY location (for PCA and the avenanthramides). The weather patterns at Sturgeon Bay are moderated by its position on a peninsula in Lake Michigan. Daily average high, low and mean temperatures during the growing season are typically 2 to 4°C lower than those at the other locations except for Ashland, which is adjacent to Lake Superior. The low morning temperatures at Sturgeon Bay are often accompanied by fog.

Cultivar differences for AOA, CA, VAN, FA, FD, AVA, AVB, and AVC concentrations indicate that it would be possible to select for these quantitative traits in a cultivar development program. However, the significant effects of environment and the interactions between environment and genotype must be considered. The HPLC analysis of the spectrum of individual phenolic components is a time consuming and costly process. Total free phenolic content, measured as GA equivalents with the Folin & Ciocalteau phenol reagent may be used as an inexpensive, easy predictor of the level of AVA , AVB , and AVC and sum of AVA, AVB, and AVC . The concentrations of the simple phenolics in the soluble fraction are so low as compared with the avenanthramides that their contribution to total free phenolic content is almost negligible.

In summary, this study confirms the high concentrations of three avenanthramides in oat relative to soluble simple phenolics. Both cultivar and location affected concentrations of some phenolic substances, but antioxidant activities differed only among cultivars. Location had the greatest effect on the avenanthramide concentrations, with unusually high levels found at Sturgeon Bay. This effect was consistent for three growing seasons. Dane always had lower concentrations of avenanthramides than Belle and Gem. A more extensive evaluation is under way to determine the ranges of avenanthramide concentrations in oat germplasm. This germplasm is available for plant breeding. This extended evaluation may lead to a study of heritability of these traits and quantitative trait loci (QTL) mapping. Extensive testing across years and locations would be desirable to select from among an elite group of genotypes those with the most favorable characteristics.


   NOTES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 NOTES
RESULTS AND DISCUSSION
 REFERENCES
 
1 Names are necessary to report factually on available data; however, the USDA neither guarantees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable. Back

Received for publication August 14, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 NOTES
 RESULTS AND DISCUSSION
 REFERENCES
 




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