Genetic Diversity of Individual Phenolic Acids in ... - ACS Publications

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Genetic Diversity of Individual Phenolic Acids in Barley and Their Correlation with Barley Malt Quality Shengguan Cai,† Zhigang Han,† Yuqing Huang, Zhong-Hua Chen, Guoping Zhang, and Fei Dai* Department of Agronomy, Zhejiang Key Lab of Crop Germplasm, Zhejiang University, Hangzhou 310058, China S Supporting Information *

ABSTRACT: Phenolic acids have been quite extensively studied in food science research because of their antioxidative effect. In this study, the genotypic difference and genetic control of phenolic acids, and their correlation with malt quality, were investigated in barley. Ferulic acid (FA) and p-coumaric acid (p-CA) were identified as two main phenolic acids, showing wide variations among 68 barley genotypes. The mean content of FA and p-CA were 2.15 μg g−1 and 1.10 μg g−1 in grains and 4.07 μg g−1 and 1.44 μg g−1 in malt, respectively. After malting, FA and p-CA were increased significantly in 55 and 37 genotypes and were reduced in 2 and 14 genotypes, respectively. Both malt FA and p-CA were positively correlated with soluble N content and Kolbach index and negatively correlated with malt extract and viscosity. The results indicated that the effect of malting on the change of an individual phenolic acid is genotype independent. Association mapping identified that 8 markers on Chromosomes 1H, 2H, 4H, and 7H are associated with grain p-CA and 4 markers on Chromosomes 3H and 7H are linked with grain FA. However, only a single marker on Chromosome 3H was found to be associated with malt FA. Moreover, a lack of overlapping markers between grain and malt indicated the genetic diversity of phenolic acids in barley grain and malt. Our results strengthen the understanding of phenolic acids in barley and their responses to the malting process. KEYWORDS: association mapping, barley (Hordeum vulgare L.), malt, phenolic acid

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INTRODUCTION Phenolic compounds are vital for food and beverages due to their strong antioxidant activities and ability to scavenge free radicals and break radical chain reactions.1 In recent years, many studies have connected the consumption of polyphenolrich foods with the prevention of chronic inflammation, cardiovascular diseases, cancers, and diabetes.2 Phenolic compounds also function as antioxidant substances and plant growth regulators in plant metabolism.2−4 Barley is a widely consumed cereal, mainly as animal feed and malt,5 which is a raw material for the beer and spirit industry.6 Both barley grain and malt contain high levels of antioxidative compounds, including phenolic acids (e.g., benzoic and cinnamic acid derivatives), flavonols, tannins, proanthocyanidins, and amino phenolic compounds.7,8 Recently, barley has gained renewed interest as an ingredient for the production of functional foods and beverages.9−12 Ferulic acid (FA) and p-coumaric acid (p-CA), usually found in the husk and aleurone layer, are the main phenolic acids in barley.13,14 Wide phenotypic variation in phenolic acid content is present among barley genotypes15,16 and is related to key agronomic traits, such as hull adherence and grain color.17,18 These compounds occur in different forms, including free, soluble conjugate and insoluble, bound forms.19 Insoluble, bound phenolic acid can be released by acid or alkali hydrolysis.20 However, during brewing, water is used as the extract solvent so that only soluble phenolic compounds are present in malt extract.21 Therefore, it is meaningful to investigate the fate of free phenolic acids during malting and brewing. Several studies have investigated the effect of malting on total polyphenols and antioxidant activity.22−24 It has been reported © 2015 American Chemical Society

that malt had higher antioxidant activity and total polyphenolic content than its corresponding barley grain from the same genotype.25 Moreover, several studies have focused on changes of individual phenolic compounds during malting. Leitao et al. (2012)26 found that malting significantly increases the contents of FA, p-CA, and sinapic acid but reduces the contents of catechin, prodelphinidin B3, and procyanidin B3. In contrast, Dvořaḱ ová et al. (2008a, b)27,28 reported that free p-CA decreased in all five cultivars and that FA decreased in only one cultivar, Bojos. We assume that the changing pattern of an individual phenolic compound may be a result of genetic variation among genotypes. However, the examination of a limited number of cultivars in these studies was not able to draw a convincing conclusion. Therefore, the effect of malting on the change of phenolic acids requires a thorough evaluation using more genotypes with wider genetic diversity. It is well-documented that polyphenols play important roles in mashing and brewing.29 These compounds can actively control oxidative reactions and extend the shelf life of beer by acting as free radical scavengers, reducing agents, and metal ion chelators.30,31 Approximately 80% of the phenolics in beer originate from malt with catechin, epicatechin, FA, p-CA, and vanillic acid being the most commonly found compounds.32 Of these phenolic compounds, FA and p-CA can be transformed into the highly flavor-active volatile phenols 4-vinylguaiacol (4VG) and 4-vinylphenol (4VP), which abate beer flavor stability.29,33,34 Malt quality parameters, such as diastatic power, malt extract, Kolbach index, and viscosity, are key indicators of Received: April 10, 2015 Accepted: July 14, 2015 Published: July 15, 2015 7051

DOI: 10.1021/acs.jafc.5b02960 J. Agric. Food Chem. 2015, 63, 7051−7057

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Journal of Agricultural and Food Chemistry mashing and brewing quality.35,36 In finger millet [Eleucine coracana (L.) Gaertn.], Siwela et al. (2010)37 found that phenolics are positively correlated with diastatic power and amylase, whereas Chethan et al. (2008)38 reported an opposing result that phenolic compounds are detrimental to malt quality due to their inhibitory effect on malt amylase. However, there has been no report on the relationships between phenolics and these parameters in barley malt. The genetic control of polyphenol has been intensively investigated in pear,39 cider apple,40 tomato,41 sorghum,42 rice,43 and barley.44 Most studies were limited to determining the total polyphenol content and did not consider individual phenolic compounds. Phenolic acids represent only a small portion of total polyphenols. Thus, any identified quantitative trait loci (QTLs) associated with total polyphenol could not be linked to an individual phenolic acid, which may potentially be the key ingredient for the brewing industry and functional foods. Modification of the biosynthesis pathway and breeding barley for high accumulation of economically important phenolic acids will only be possible after the identification of QTLs or genes for individual phenolic acids and by understanding the links between phenolic acids and malt quality. Accordingly, the aims of this study were (1) to determine the relationship between barley grain and corresponding malt in their content of individual phenolic acids in 68 barley genotypes, (2) to investigate the potential relationship between individual phenolic acids and malt quality, and (3) to identify QTLs associated with content of the key phenolic acids in barley grain and malt.

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Determination of Phenolic Acids by High-Performance Liquid Chromatography. Measurement of phenolic acid content was carried out by high-performance liquid chromatography (HPLC) analysis with an Agilent 1260 Liquid Chromatograph (Agilent, Santa Clara, USA). Separation was performed with a Diamonsil 5u C18 (250 × 4.6 mm) column (Dikma, China) at 40 °C. Elution was performed using a gradient procedure with a mobile phase containing Solvent A (0.1% formic acid in water) and Solvent B (methanol) through the following steps: 0 min, 30% B; 10 min, 45% B; 20 min, 50% B; 25 min, 80% B; 32 min, 30% B; 37 min, 30% B. The total run time was 37 min at a solvent flow rate of 0.8 mL min−1 and with a 15 μL injection volume. The content of the individual phenolic compound in the extracts was calculated using a standard curve. Association Mapping of Individual Phenolic Acids. Association analysis between 758 DArT markers and phenolic acids was performed using TASSEL v3.0 (http://www.maizegenetics.net). Three different models were employed in the association analysis according to a previous study with some modifications.48−50 The structure matrix and kinship were included as a covariate to correct the population structure in the model y = Xβ + Qν + Zμ + e, where X is the DArT marker matrix, Q is the structure matrix, Z is the kinship matrix, β and ν are coefficient vectors for DArT marker and population structure, respectively, μ is a vector of random genetic effects [μ ∼ N (0, 2 K)], and e is the random error vector. Other models including only the structure matrix or kinship were also applied in the association analysis. These models are as follows: y = Xβ + Zμ+ e, and y = Xβ + Qν + e. For the fitness and efficiency of different models to be evaluated, the quantile-quantile (Q-Q) plot was displayed using TASSEL v3.0. The Benjamini−Hochberg false discovery rate (BHFDR) of P < 0.01 was applied in association with a significance test. Statistical Analysis. Person correlation index among grain and malt phenolic acids and between malt phenolic acids and malt quality parameters were calculated using SPSS 19.0 (SPSS Inc., Chicago, USA). One-way ANOVA with the Tukey method was employed in a significance test using SPSS 19.0.

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MATERIALS AND METHODS

Plant Materials. Sixty-eight barley genotypes (Supplementary Table 1, Supporting Information) were planted in the field of the experimental farm at Zhejiang University, Huajiachi campus, Hangzhou, China (Hangzhou, 120.2°E, 30.5°N). All of these genotypes are hulled barley with only one genotype, Xindengmenggumai, being a hulless barley. Each genotype was sown in a 2 m row with 0.25 m between rows with three replications. Field management, including fertilization, weed, and disease control, were the same as that applied locally. At maturity, barley grains were harvested and stored in a cool room at 4 °C.45,46 Grain samples (150 g) were micromalted in a Phoenix System Micromalting Apparatus (John & White, Adelaide, Australia) according to the method described by Dai et al. (2007)45 and Dvořaḱ ová et al. (2008b)28 with some modifications. The procedure for the malting process was as follows: (1, steeping stage) 5 h of wet stage at 17 °C, 8 h of air-rest stage at 17 °C, 8 h of wet stage at 16 °C, 12 h of air-rest stage at 16 °C, 4 h of wet stage at 15 °C, 5 h of air-rest stage at 15 °C, and 2 h of wet stage at 15 °C; (2, germination stage) 48 h of germination at 16 °C and 48 h of germination at 15 °C; (3, Kilning stage) 2 h at 50 °C, 4 h at 55 °C, 6 h at 60 °C, 4 h at 65 °C, 1 h at 70 °C, 1 h at 75 °C, 1 h at 80 °C, and 2 h at 82 °C. The malt was stored at 4 °C for further analysis. The barley grains and malt were finely ground and fitted with a 0.5 mm screen. Extraction of Phenolic Acids. The procedure for extraction of phenolic acids was based on that described by Zhao et al. (2006)47 with some modification. Two hundred milligrams of ground sample was sonicated (40 kHz, 120 W) for 40 min with 4 mL of 80% methanol (v/v) at 70 °C. After centrifugation (5,000 g for 15 min), the supernatant was collected and freeze-dried in a vacuum freezing dryer. The residue was redissolved in 250 μL of 70% methanol (v/v) and filtered through a 0.45 μm membrane. The filtrate was transferred to 2 mL autosampler vials (Agilent, Santa Clara, USA) equipped with 200 μL glass inserts.

RESULTS Genotypic Diversity of Phenolic Acid Content in the Grain and Malt of Barley. Two types of phenolic acids, FA and p-CA, were identified in all of the genotypes (Supplementary Table 1, Supporting Information), except for p-CA in Xindengmenggumai, a hulless barley. The mean content of FA and p-CA in the grains were 2.15 μg g−1 (ranging from 1.13 to 4.04 μg g−1) and 1.10 μg g−1 (ranging from 0.19 to 3.53 μg g−1), respectively (Table 1, Figure 1). The mean content of pTable 1. Descriptive Statistics of Phenolic Acids in Grain and Malta min median max mean CV

p-CA in grain

FA in grain

p-CA in malt

FA in malt

0.19 0.97 3.53 1.10 0.48

1.13 1.94 4.04 2.15 0.33

0.65 1.36 3.56 1.44 0.40

1.64 3.99 11.27 4.07 0.40

a

p-CA: p-coumaric acid. FA: ferulic acid. CV: coefficient of variation. The units for the phenolic acids are μg g−1.

CA in malt was 1.44 μg g−1, ranging from 0.65 to 3.56 μg g−1, which was similar to those in grains (Table 1, Figure 1). However, the average content of FA at 4.07 μg g−1 in malt was nearly double that in the grains, including the highest FA content at 11.27 μg g−1 found in the malt of genotype, Belae (Table 1, Figure 1). The coefficient of variation (CV) for FA and p-CA content was 0.48 and 0.33, respectively (Table 1). 7052


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Figure 1. Distribution of phenolic acids in grain and malt among 68 genotypes for (a) p-CA in grain, (b) FA in grain, (c) p-CA in malt, and (d) FA in malt.

Correlation of FA and p-CA Content in Barley Grain and Malt. There were significant and positive correlations between FA and p-CA in grains (r = 0.758, P < 0.01, n = 67) and in malt (r = 0.745, P < 0.01, n = 68) (Table 2). However,

malt and six malt quality parameters, including diastatic power, malt extract, Kolbach index, viscosity, and soluble and total N content.51 The two phenolic acids were positively correlated with Kolbach index (r = 0.496 and r = 0.393 for p-CA and FA, respectively) and soluble N (r = 0.539 and r = 0.307, respectively). Negative correlations between p-CA and FA with malt extract (r = −0.283 and r = −0.271, respectively) and viscosity (r = −0.299 and r = −0.408, respectively) were also observed (Table 3). Association Analysis of DArT Markers and Phenolic Acids in Grains and Malt. The content of phenolic acids in grains and malt and 758 DArT markers were used to perform association mapping. Q-Q plots showed that the k model has the best fit to the association analysis (Supplementary Figure 1, Supporting Information). A total of 13 markers were identified to be significantly associated with phenolic acids (Table 4). Twelve molecular markers were found in grain, but only one was identified in malt. Eight markers on Chromosomes 1H, 2H, 4H, and 7H were associated with p-CA in grain, and 4 markers on Chromosomes 3H and 7H were associated with FA in grain. Marker bpb-3484 on Chromosome 7H was found to be associated with both FA and p-CA in grain. Additionally, a marker on Chromosome 3H was associated with FA in malt. Each of these markers could account for 15.7−22.7% of the phenotypic variation. Moreover, the marker associated with FA in malt, bpb-9583, was located at 6.0 cM of 3H, independent of any locus linked to FA in grains (Table 4), suggesting a large impact of malting on the content of phenolic acids.

Table 2. Correlation Analysis of Phenolic Acids in Barley Grains and Malt FA in grain p-CA in malt FA in malt a

p-CA in grain

FA in grain

p-CA in malt

0.758a 0.092 0.044

−0.002 0.043

0.745a

Significant correlation at the P < 0.01 level.

no significant correlation of FA or p-CA was found between grain and malt of barley. For determining the effect of malting on phenolic acid content, the difference of phenolic acid content between grains and malt was evaluated by one way ANOVA analysis. After malting, p-CA increased significantly in 37 genotypes and was reduced in 14 genotypes (Figure 2; Supplementary Table 1, Supporting Information). Fifty-five genotypes exhibited a remarkable increase in FA content after malting, whereas the FA content of two genotypes was reduced (Figure 2; Supplementary Table 1, Supporting Information). The ratios of grains to malt ranged from 0.39 to 8.65 for p-CA among all genotypes and from 0.68 to 6.28 for FA (Figure 2; Supplementary Table 1, Supporting Information), indicating that the effect of malting on phenolic acid is highly genotype independent. Phenolic Acids Are Associated with Malt Quality. Correlation analysis was conducted between phenolic acids in 7053


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Table 4. DArT Markers with a Significant Marker-Trait Associationa trait

marker

chromosome

genetic position (cM)

p-CA in grain

bPb-4909

1H

72.9

0.0086

0.157

bPb-0631 bPb-1959 bPb-6822 bPb-8949 bPb-1469 bPb-0027 bPb-3484 bPb-9746

1H 1H 2H 2H 4H 7H 7H 3H

128.5 133.1 114.4 122.3 14.6 111.7 133.4 54.8

0.0071 0.0056 0.0018 0.0034 0.0039 0.0056 0.0026 0.0074

0.165 0.175 0.227 0.204 0.198 0.176 0.210 0.163

bPb-6347 bPb-7156 bPb-3484 bPb-9583

3H 7H 7H 3H

55.6 27.2 133.4 6.0

0.0053 0.0083 0.0061 0.0054

0.197 0.158 0.172 0.178

FA in grain

FA in malt

P value

R2 (marker)

a These markers were identified using the k model. The significance test for association analysis is P < 0.01. R2 (marker) denotes the contribution of the marker for phenotypic variation.

Figure 2. Changes of phenolic acids in grain and their corresponding malt for each genotype for (a) p-CA and (b) FA. The left and right point of each line (between two boxplots) represents the content of phenolic acid in grain and the corresponding malt, respectively. Red and blue lines represent a significant increase and decrease in the phenolic acid after the malting process, respectively. Gray lines represent no significant difference between the content of phenolic acid in grain and that in malt.

corresponding malts to investigate the genotypic difference of the effect of the malting process on individual phenolic acids. Most of the genotypes exhibited a notable increase in the contents of FA and p-CA after malting. The increase may be attributed to the effect of the Maillard reaction during the early stage of the kilning process, which leads to enzymatic release of extractable bound phenolics in the matrix.52,54−56 For example, ferulic acid esterase is released during the germination and early kilning steps of the malting process, thus facilitating the release of bound FA associated with lignin and arabinoxylans.57,58 Similar results have been reported on the effect of the germination process on phenolic acid in rice.59,60 Shibuya (1984)59 reported that free phenolics increased in germinated brown rice due to dismantling of the cell wall. Tian et al. (2004)60 found that bound phenolic compounds were released during the germination of rice due to carbohydrase enzymes hydrolyzing the endosperm. However, a decrease in the content of malt phenolic acid was observed in a few genotypes (2 and 14 genotypes for FA and pCA, respectively) in this study, as well as in some previous reports.27,28 The reason for this decrease could be due to leaching of phenolic compounds into the steeping water61 or due to formation of insoluble complexes with proteins.62 High kilning temperature in the late stage of the kilning process may also lead to degradation of phenolic compounds.56 Phenolic acids exhibited a complex change during the malting process.25 However, it remains unknown whether these compounds have an impact on barley malt qualities, such as diastatic power, malt extract, viscosity, Kolbach index, and soluble and total N. To our knowledge, this study is the first attempt to investigate the causal relationships between individual phenolic acids and these malt quality indicators. The current experiment employed 68 genotypes (Supplementary Table 1, Supporting Information) to ensure the representativeness and reliability of the results. The phenolic acids showed significant and positive correlations with soluble N and Kolbach index (Table 3). Obviously, the malt extract with high soluble N is rich in hydrolytic enzymes (i.e., esterase),

Table 3. Correlation Analysis of Malt Phenolic Acids and Malt Quality Parameters diastatic power Kolbach index malt extract viscosity soluble N total N

p-CA

FA

0.236 0.496b −0.283a −0.299a 0.539b 0.230

0.060 0.393b −0.271a −0.408b 0.307a 0.097

a

Significant correlation at P < 0.05 level. bSignificant correlation at P < 0.01 level.

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DISCUSSION Barley and malt contain a large number of antioxidant compounds, such as phenolics, ascorbic acid, phytic acid, and melanoidins, which can impact beer stability.52 Of these, polyphenol and melanoidins are the main sources of natural antioxidants, which originate from either raw barley or malting processes.53 Malting processes, including steeping, germination, and kilning, have a huge effect on the fate of endogenous phenolic compounds.25 It was found that malt always has a higher total polyphenol content as well as higher antioxidant activity than corresponding barley grains, suggesting that the malting process results in an increase in the antioxidant activity and total polyphenols.24,25 However, controversial results were documented regarding the changes of individual phenolic compounds during the malting process.26−28 In this study, we determined the contents of two main phenolic acids, FA and p-CA, in 68 barley genotypes and 7054


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Journal of Agricultural and Food Chemistry facilitating the release of phenolic acids.57,58 These hydrolytic enzymes can modify the endosperm to liberate some of the bound phenolic compounds during germination.63 Conversely, the phenolic acids were significantly and negatively correlated with malt extract and viscosity. It is well-known that phenolic acids are mainly located in the husk and aleurone layer.13,14 Thus, we proposed that the genotypes with more husk and/or aleurone (in another words, fewer endosperm) might contain a higher content of phenolic acids, and fewer endosperm will obviously lead to a lower malt extract. An extreme example is that the p-CA content of a hulless genotype, Xindengmenggumai, was below the detection limit of HPLC analysis. This result was in agreement with the observation that hulled barley has a higher content of phenolic acid than dehulled barley.17 Identifying QTLs and genes controlling phenolic acids in barley grain and malt could improve the understanding of the molecular genetic basis of phenolic acid metabolism. The results of association mapping indicated that phenolic acids in barley grain are polygenic traits. Although QTLs associated with total polyphenol content have been identified in barley,44 none of them are colocated with the QTLs detected in the present study. This could be due to the fact that QTLs of total polyphenol content are not likely to be responsible for the genetic variation in the individual phenolic acids. As phenolic acids only represent a small portion of total polyphenols, which also include flavonoids, tannins, and anthocyanins. Interestingly, p-CA associated marker bpb-8949 (122.3 cM, 2H) colocalized with the major QTL (119−125 cM, 2H) controlling polyphenol oxidase (PPO) activity.44,64,65 PPO enzyme functions to catalyze the oxidation of phenolic substrates to quinines; therefore, its activity could influence the content of the phenolic compound.66,67 This may explain the colocalization of QTLs for p-CA and PPO. The barley genomic information facilitates the identification of probable candidate genes based on QTL results.68 The sequences of DArT markers were obtained from the Web site of Diversity Array Technology Pty Ltd. (http://www. diversityarrays.com). These sequences were used to search the corresponding contigs in the IPK barley genome database, some of which contain genes with annotations (http:// webblast.ipk-gatersleben.de/barley). Interestingly, the sequence of marker bpb-0027 was found to match contig_137941, which contains the cytochrome P450 (CYP73 encoding cinnamate 4hydroxylase) gene. It has been well-established that cytochrome P450 catalyzes cinnamic acid to p-CA in the phenylpropanoid pathway, leading to the biosynthesis of lignin and numerous other phenolic compounds in plants.69,70 Another search for the sequence of marker bpb-7156 was found to match contig_51262, which contains the oxidoreductase gene. Oxidoreductases, such as PPO and peroxidase (PDX), play vital roles in the regulation of the phenolic content of virgin olive oil.71 These identified genes may participate in phenolic acid metabolism; however, the functions of these genes need to be studied thoroughly using transgenic approach in the future. It is worth noting that marker bpb-3484 is associated with both FA and p-CA, indicating that the two phenolic acids could be tightly linked or even likely be controlled by the same group of genes. This hypothesis was partially supported by the highly positive correlations between the contents of the two phenolic acids. Conversely, the results provide some insights into understanding of the molecular mechanisms controlling the two traits. The lack of any common marker between grain and malt phenolic acids is consistent with the finding that there is

no correlation between grain and malt for this trait. Moreover, our results may provide some preliminary genetic evidence for the significant effect of the malting process on phenolic acid metabolism.

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ASSOCIATED CONTENT

* Supporting Information S

FA and p-CA concentrations and malt/grain ratios in 68 barley genotypes and quantile-quantile plots of estimated and expected log10(P) values. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.5b02960.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected], Phone: +86 571 88982115, Fax: +86 571 88982117. Author Contributions †

S. C. and Z. H. contributed equally to this work.

Funding

This study was supported by the Natural Science Foundation of China (31201166, 31471480, and 31401369) and the Fundamental Research Funds for the Central Universities. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Ms. Jingqun Yuan and Mei Li, technicians of the 985Institute of Agrobiology and Environmental Sciences of Zhejiang University, for assistance in HPLC analysis and Ms Michelle Mak (University of Western Sydney, Australia) for English language editing.

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REFERENCES

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