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. 2024 Feb 28;103(5):103590. doi: 10.1016/j.psj.2024.103590

Genome-wide association studies of anserine and carnosine contents in the breast meat of Korean native chickens

Minjun Kim *,1, Jean P Munyaneza *,1, Eunjin Cho †, Aera Jang ‡, Cheorun Jo §, Ki-Chang Nam ǁ, Hyo Jun Choo , Jun Heon Lee *,†,2
PMCID: PMC11067755  PMID: 38457991

Abstract

Histidine-containing dipeptides (HCDs), such as anserine and carnosine, are enormously beneficial to human health and contribute to the meat flavor in chickens. Meat quality traits, including flavor, are polygenic traits with medium to high heritability. Polygenic traits can be improved through a better understanding of their genetic mechanisms. Genome-wide association studies (GWAS) constitute an effective genomic tool to identify the significant single-nucleotide polymorphisms (SNPs) and potential candidate genes related to various traits of interest in chickens. This study identified potential candidate genes influencing the anserine and carnosine contents in chicken meat through GWAS. We performed GWAS of anserine and carnosine using the Illumina chicken 60K SNP chip (Illumina Inc., San Diego, CA) in 637 Korean native chicken-red-brown line (KNC-R) birds consisting of 228 males and 409 females. The contents of anserine and carnosine in breast meat of KNC-R chickens were investigated. The mean value of the anserine and carnosine are 29.12 mM/g and 10.69 mM/g respectively. The genomic heritabilities were moderate (0.24) for anserine and high (0.43) for carnosine contents. Four and nine SNPs were significantly (P < 0.05) associated with anserine and carnosine, respectively. Based on the GWAS result, the 30.6 to 31.9 Mb region on chicken chromosome 7 was commonly associated with both anserine and carnosine. Through the functional annotation analysis, we identified HNMT and HNMT-like genes as potential candidate genes associated with both anserine and carnosine. The results presented here will contribute to the ongoing improvement of meat quality to satisfy current consumer demands, which are based on healthier, better-flavored, and higher-quality chicken meat.

Key words: Korean native chicken, meat flavor, genome-wide association study, candidate gene, histidine-containing dipeptide

INTRODUCTION

Chicken meat is very popular among meat consumers because of its health benefits and affordable price (Munyaneza et al., 2022). Although chicken meat is already preferred over other types of meat by consumers (Marangoni et al., 2015), there has been increasing interest in improving the meat quality of chickens to meet consumer demands, especially higher-flavored meat (Kim et al., 2023). Meat quality traits can be divided into visual (appearance) quality, eating quality, and reliance quality traits (Ismail and Joo, 2017). These traits affect the decision of consumers when purchasing the meat (Jayasena et al., 2013; Ismail and Joo, 2017). The meat of native chickens has a special taste and aroma because of the high content of flavor precursors; thus, native chicken meat is usually chosen over the meat of broilers (Jayasena et al., 2014). The Korean native chicken-red-brown line (KNC-R) is one of 5 Korean native chicken lines, which are classified based on the color of their plumage (Jung et al., 2013). Compared with the other lines, the KNC-R has a higher body weight and contains more flavor precursors, including histidine-containing dipeptides (HCDs) such as carnosine (Jung et al., 2013).

After tenderness, meat flavor is the most important eating quality trait that influences consumer choice (Ismail and Joo, 2017; Munyaneza et al., 2022). There are many flavor precursors present in fresh meat; these precursors including nucleotides, amino acids, organic acids, sugars, and HCD (anserine and carnosine) (Jayasena et al., 2013; Jung et al., 2013; Uemoto et al., 2017). These precursors are stimulated by heat during the cooking process to produce the final flavor (Jayasena et al., 2013; Jayasena et al., 2014; Ismail and Joo, 2017; Shahidi and Hossain, 2022). Carnosine is an HCD that is abundant in mammals, such as beef cattle and pigs, whereas anserine is abundant in nonmammalian species, such as chickens (Jung et al., 2013). Carnosine is synthesized in the body by bonding 2 amino acids, β-alanine and L-histidine (Blancquaert et al., 2016). Anserine is the methylated analog of carnosine (Jung et al., 2013; Blancquaert et al., 2016). Anserine and carnosine have various functions such as antioxidants (Jung et al., 2013; Blancquaert et al., 2016) and the umami taste (Dashdorj et al., 2015). Carnosine improves various meat quality traits such as redness and drip loss, and pH (Ma et al., 2010).

The selection and breeding of animals with high HCD contents is the best method to produce highly flavored meat. Thus, identification of the potential candidate genes for anserine and carnosine in chickens is vital because it provides crucial information required to breed chickens with highly flavored meat. Carnosine and anserine reportedly have moderate to high heritabilities (0.383 for carnosine and 0.531 for anserine in Angus cattle), indicating genetic effects on carnosine and anserine contents in muscle (D'Astous-Pagé et al., 2017).

A few genes have been associated with anserine and carnosine contents in chickens, including genes related to carnosine synthesis (carnosine synthase 1: CARNS1), carnosine hydrolysis (carnosine dipeptidase1: CNDP1), carnosine transport (solute carrier family 15 member1: SLC15A1), and beta-alanine transport (solute carrier family 6 member 6: SLC6A6) (Everaert et al., 2012). Genome-wide association studies (GWAS) was used in chickens to identify potential candidate genes related to growth traits, dry matter, intramuscular fat, meat color, skin color, and abdominal fat (Xie et al., 2012; Sun et al., 2013). Although GWAS is considered an effective tool to identify potential candidate genes for polygenic traits in farm animals, including chickens, no GWAS have been conducted to identify the various genes influencing anserine and carnosine contents in chickens. Therefore, this study was performed to identify candidate genes influencing the anserine and carnosine contents in the breast meat of KNC-R chickens through GWAS.

MATERIALS AND METHODS

Ethics Approval

The protocols for animal experimentation in this study were approved by the Institution of Animal Care and Use Committee of the National Institute of Animal Science (NIAS) (Approval number: NIAS 20212219) and the Animal Ethics Committee of Chungnam National University (202209A-CNU-141) to meet the global animal welfare guidelines.

Chicken Population

This study used a total of 637 KNC-R chickens (males, n = 228 and females, n = 409) kept under the same feeding and management conditions at the Poultry Research Institute of the NIAS in Pyeongchang, South Korea. A battery cage system was used to raise chickens, and commercial feed was provided (starter and grower). Feed and water were provided ad libitum. Blood samples were collected from wing blood vessels and kept at -20℃ until DNA extraction. All birds were euthanized at 10 wk. For the analysis of anserine and carnosine contents in KNC-R chickens, we collected a 100 g sample of breast tissue from each bird and kept it at -80℃ until analysis.

Phenotype Measurement and Preprocessing

We used nuclear magnetic resonance spectroscopy, as described by Kim et al. (2021), to analyze the anserine and carnosine contents from 637 breast samples of KNC-R chickens. The anserine and carnosine contents were expressed in units of mM/g. After normalizing the phenotypic data with logarithm, cube, or square root scaling methods, the normalizing method with the highest Shapiro-Wilk P-value was used for further analysis. A data trimming procedure was performed; values larger or smaller than 3 standard deviations were regarded as outliers and removed from the analysis. Consequently, 635 and 631 samples from the anserine and carnosine data were used for the association analysis respectively. We used the R software v4.2.1 (R Core Team, 2022) to preprocess our data.

Genotyping and Preprocessing

We extracted DNA from blood by using a commercial kit (GeNet Bio, Korea). An Illumina chicken 60K single-nucleotide polymorphism (SNP) chip (Illumina Inc.) was used to generate the genotypic data, which contained 57,636 SNPs from the extracted DNA samples. The generated SNP chip data is available as supplementary material. PLINK1.9 software (Purcell et al., 2007) was used to filter genotypic data. SNPs with a call rate < 0.9, minor allele frequency < 0.01, and Hardy–Weinberg test P-value < 1 × 10−6 were removed from the analysis. Then, principal component analysis (PCA) was conducted using the filtered variants to see the population structure. Finally, 44,842 variants remained and were used for the association test.

Construction of the Genomic Relationship Matrix and GWAS

We used the Genome-wide complex trait analysis (GCTA) software (Yang et al., 2011) to construct the genomic relationship matrix of 637 birds before the performance of GWAS. According to samples of preprocessed phenotype data for each trait, samples of genotype and genomic relationship matrix were used for analysis. The restricted maximum-likelihood (REML) analysis function in GCTA software was used to estimate the heritabilities and genetic variance of anserine and carnosine.

The mixed linear model of GCTA, based on the leave-one-chromosome-out method (MLMA-LOCO), was used to perform GWAS. The following mathematical model was used in the association analysis:

y=a+bx+g−+e

where y is the phenotypic value corrected by covariates; a is the mean of the phenotypic records; b is the additive effect of the tested SNP marker; x is the genotype of the SNP; g- is the effect of all SNPs that were calculated using the genetic relationship metrics, except for SNPs on the chromosome undergoing analysis; and e is the residual effect vector. The sex, generation group, and carcass weight of each animal were used as covariates, along with principal components 1 and 2 of a PCA according to genotype. After the analysis, the tested SNPs were assessed using the Bonferroni-corrected P-value, with a 5% significance threshold, to identify significantly associated SNPs. The results were visualized by summarizing the trend of marker significance in a Manhattan plot. The significant genomic region of a trait was defined as the overlapped regions from 500 kb upstream and downstream of each significant SNP position on GRCg6a, annotated using the 106-version genome from the Ensembl database. Candidate genes were then selected for traits according to their functions.

The effect size of each SNP marker was defined as the contribution of the SNP to the genetic variance of the trait. The following model was used to estimate the effect size of each SNP:

ES=2b2p(1−p)/V(g)

where ES is the estimated effect size of the tested SNP, p is the minor allele frequency of the tested SNP, and V(g) is the total genetic variance of the trait.

Functional Annotation Analysis

We used the BioMart web-based tool (Kinsella et al., 2011) of the Ensembl database to extract genes located in the significant genomic region of the chicken reference genome GRCg6a. The identified genes were used for functional analysis. The annotations of Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways were analyzed for genes in the significant region, using the ClusterProfiler package (Yu et al., 2012) in R software. We used a significance threshold of (P < 0.05) for enriched KEGG pathways. Additionally, we searched for gene functions reported in the literature.

RESULTS

General Descriptive Statistics

The descriptive statistics for the anserine and carnosine contents in KNC-R breast meat are summarized in Table 1. Figure 1 summarizes the phenotypic values in the histogram, box plot, and quantile-quantile plot. Comparison of the mean values for phenotypic data showed that the anserine content was higher than the carnosine content in KNC-R breast meat. The mean anserine and carnosine contents were approximately 29.12 and 10.69 mM/g, respectively. Cube and square root transformation methods were used to normalize the phenotypic values of anserine and carnosine, respectively. Anserine had a moderate heritability of 0.24, whereas there was a high heritability for carnosine (0.43) as shown in Table 1. The PCA showed that the first and second principal components explained 6.495% and 6.331% of the total variance of SNP markers. The PCA indicated that the experimental population did not show a population stratification (Supplementary Figure S1).

Table 1.

Descriptive statistics and heritability estimates of anserine and carnosine compound traits measured in chicken breast meat (unit: mM/g).

Traits Mean SD1 CV2 (%) Minimum Maximum Heritability
Anserine 29.1178 4.2188 0.1449 11.6894 39.6486 0.2402
Carnosine 10.6894 3.0798 0.2881 2.5485 26.6377 0.4386
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1

SD: standard deviation.

2

CV: coefficient of variation.

Figure 1.

Figure 1

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Phenotype distributions of anserine and carnosine contents in chicken breast meat. Histogram, box plot, and quantile-quantile plots of (A) anserine and (B) carnosine contents in chicken breast meat.

GWAS Results and Significant Genomic Region

The four SNPs were significant (adjusted P < 0.05) for the anserine trait according to the Bonferroni-corrected genome-wide significance threshold. Significant SNPs were positioned at 31.1 to 31.4 Mb on chromosome 7. The most significant SNP was rs317734561 (P = 2.82 × 10−8), which was located at 31,123,992 bp on chromosome 7. Based on the positions of the detected SNPs, the significant genomic region was defined as 30,623,992 to 31,951,894 bp on chromosome 7. Nine SNPs were significant (adjusted P < 0.05) for the carnosine trait. The detected SNPs were located at 30.2 to 31.5 Mb on chromosome 7. The most significant SNP in the carnosine trait was rs312271662 (P = 4.38 × 10−9), which was the second most significant marker in the anserine trait. No other significant SNPs were common in both traits, according to the GWAS results. The significant genomic region for the carnosine trait was defined as the 29,668,946 to 32,048,253 bp region on chromosome 7. Notably, the genomic region for the anserine trait was completely covered by the region for the carnosine trait. No other genomic regions were significant according to the GWAS results. Further functional annotation analysis was performed using the significant genomic region for anserine. Manhattan plots and detailed GWAS results for each SNP are shown in Figure 2 and Table 2, respectively. All positional information was obtained from GRCg6a, annotated using the 106-version genome from the Ensembl database.

Figure 2.

Figure 2

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Genome-wide Manhattan plots of the -log10(P-value) for significant single-nucleotide polymorphisms (SNPs). (A) and (B) show the association test results for anserine and carnosine contents, respectively. The x-axis indicates chromosome number, and the y-axis depicts the -log10(P-value) used to indicate the significance of the tested SNPs. The red line indicates the Bonferroni-corrected 5% significance threshold. The blue dotted line indicates the physical position of the most significant SNP for each trait.

Table 2.

Significant single-nucleotide polymorphisms (SNP) of anserine and carnosine based on the genome-wide association study results.

Anserine Chr1 SNP ID Position (bp) Genotype SNP effect Genomic location P-value Freq2
7 rs317734561 31,123,992 C>T 0.2227 Intron/THSD7B 2.82e-08 0.724
7 rs312271662 31,418,979 A>G 0.1908 Intergenic 4.31e-07 0.787
7 rs16609270 31,319,528 C>T 0.1703 Upstream3/ENSGALG00000052507 8.84e-07 0.953
7 rs16609445 31,451,894 T>C 0.1850 Intron/NXPH2 9.48e-07 0.723
Carnosine Chr SNP ID Position (bp) Genotype SNP effect Genomic location P-value Freq
7 rs312271662 31,418,979 A>G 0.1378 Intergenic 4.38e-09 0.788
7 rs16608133 30,631,914 A>G 0.1279 Downstream4/R3HDM1 5.91e-09 0.459
7 rs14626540 31,348,874 G>A 0.1397 Intergenic 1.40e-08 0.482
7 rs13599357 30,922,055 G>T 0.1409 Intergenic 1.46e-08 0.662
7 rs14626854 31,548,253 G>A 0.1224 Intron/ENSGALG00000048656 6.04e-08 0.664
7 rs313962734 30,168,946 T>C 0.1117 Intergenic 1.30e-07 0.230
7 rs16607403 30,213,403 A>G 0.1098 Intron/ENSGALG00000055018 1.63e-07 0.246
7 rs13599074 30,318,241 C>T 0.1044 Intron/MGAT5 4.29e-07 0.645
7 rs14626512 31,324,709 T>C 0.0988 Intron/ENSGALG00000052507 5.20e-07 0.271
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1

Chr: chromosome.

2

Freq: reference allele frequency.

3

Upstream: upstream gene variant.

4

Downstream: downstream gene variant.

Potential Candidate Genes

The following 15 protein-coding genes were included in the significant genomic regions: C-X-C motif chemokine receptor 4 (CXCR4), aspartyl-tRNA synthetase (DARS), histamine N-methyltransferase (HNMT), lactase (LCT), LDL receptor related protein 1B (LRP1B), minichromosome maintenance complex component 6 (MCM6), neurexophilin 2 (NXPH2), R3H domain containing 1 (R3HDM1), speckle type BTB/POZ protein like (SPOPL), thrombospondin type 1 domain containing 7B (THSD7B), ENSGALG00000012382, ENSGALG00000048656, ENSGALG00000047828, histamine N-methyltransferase-like (HNMT-like: LOC771456), and UBX domain protein 4 (UBXN4).

KEGG pathway analysis was conducted using these genes, and the gga00340 (Histidine metabolism) pathway was identified with high significance (P = 3 × 10−4). The genes related to this KEGG term are HNMT and HNMT-like genes. Additionally, we searched the literature to identify candidate genes related to anserine and carnosine in chickens. This search revealed that HNMT-like and HNMT genes were candidate genes may influence the anserine and carnosine contents in chicken muscles. HNMT gene resides in the region from 31,246,874 bp to 31,261,994 bp of chromosome 7. The HNMT gene consists of 7 exons and 6 introns. The HNMT-like gene is located in the region from 31,212,705 bp to 31,221,718 bp of chromosome 7. The structure of the HNMT-like gene is eight exons and seven introns.

DISCUSSION

Meat quality traits, especially eating quality traits (e.g., meat flavor) have become important in chicken farming and breeding programs. The natural flavor of a meat is a very important trait that influences decisions by meat consumers to continue purchasing that particular meat (Ismail and Joo, 2017). GWAS have become an effective tool for improving meat quality traits because of developments in SNP chips that have allowed the identification of candidate genes influencing various traits in chickens. For example, previous GWAS researches have shown that candidate genes, including ADSL, AMPD1, and AMPD2 are associated with inosine 5′-monophosphate (Zhang et al., 2018; Munyaneza et al., 2022). SCD, FASN, ELOVL1, ADIPOQ, ADIPOR2, and ELOVL6 are associated with different fatty acids (Munyaneza et al., 2022). In this study, we performed GWAS of anserine and carnosine on KNC-R chickens; our analyses revealed candidate genes and markers for improving meat quality traits, especially meat flavor. We estimated that the heritabilities for anserine (0.24) and carnosine (0.43) were in the medium to high range, indicating the potential to improve meat flavor through genomic selection.

Carnosine was first isolated in 1900 from beef muscle by Vladimir Gulevitsch (Everaert et al., 2012; Peters et al., 2018). Anserine was first discovered in goose muscle in 1929 (Kaneko et al., 2017; Kwiatkowski et al., 2018). Both anserine and carnosine are classified as bioactive peptides because of their health benefits for humans (Mateescu et al., 2012; Barbaresi et al., 2019). The anserine and carnosine contents in meat are influenced by genetic factors (e.g., breed or line) and environmental factors (e.g., rearing conditions, type of muscle fiber, sex, and age) (Everaert et al., 2012; Jung et al., 2013). For example, Korean native chicken breast meat has greater carnosine and anserine contents than the breast meat of other lines (Jung et al., 2013). HCDs have many functions, including antioxidant, muscle pH buffering, anti-lipid oxidation, and anti-glycation activities (Jung et al., 2013; Kaneko, et al., 2017; Barbaresi et al., 2019). Because of its anti-oxidative properties, carnosine could play a major role in the treatment of type II diabetes (Artoli et al., 2018; Robin et al., 2022). Anserine and carnosine reportedly can protect humans from some cancers, Alzheimer's disease, and Parkinson's disease (Suwanvichanee et al., 2022).

We analyzed KEGG pathways to detect positional candidate genes and identify the biological pathways influencing anserine and carnosine contents in KNC-R muscles. The “Histidine metabolism” (gga00340) pathway was significantly enriched, which included the carnosine to anserine conversion process. HNMT and HNMT-like genes were belonged to this pathway. We also reviewed the literature to confirm that HNMT and HNMT-like genes are the positional candidate genes for anserine and carnosine contents in KNC-R chickens. Previous studies showed that the carnosine formation rate and content in human muscle and horse muscle are limited by the availability of β-alanine, but not L-histidine (Everaert et al., 2012; Kwiatkowski et al., 2018). The β-alanine level is affected by various transporters and enzymes (Everaert et al., 2012). In chickens, the β-alanine and L-histidine levels reportedly are rate-limiting factors for carnosine synthesis (Barbaresi et al., 2019; Suwanvichanee et al., 2022). The carnosine synthase (CARNS1), also known as ATP-grasp-domain-containing protein 1 (ATPGD1), is an enzyme that catalyzes the synthesis of carnosine from β-alanine and L-histidine (Everaert et al., 2012; Jung et al., 2013; Drozak et al., 2015; Kwiatkowski et al., 2018; Peters et al., 2018; Sharma et al., 2022).

According to the histidine metabolism pathway in chicken, histamine N-methyltransferase (HNMT) encoded by HNMT gene is related to the histamine quantity. L-histidine is metabolized to histamine by histidine decarboxylase. The HNMT catalyzes methylation of histamine producing N-methylhistamine (Brosnan and Brosnan, 2020). This implies that the HNMT activity can affect the amount of L-histidine indirectly, which is a main precursor of carnosine and anserine. Anserine is synthesized through two pathways in chickens: methylation of carnosine to anserine by carnosine N-methyltransferase, and direct synthesis from 1-methylhistidine and β-alanine (Kai et al., 2015; Kwiatkowski et al., 2018). In avian species and reptiles, carnosine-N-methyltransferase (CARMT), also known as histamine N-methyltransferase-like or carnosine N-methyltransferase 2 (CARNMT2), is encoded by the HNMT-like gene (Kwiatkowski et al., 2018). The HNMT-like gene is absent from mammalian genomes, including the human genome, in which carnosine-N-methyltransferase is encoded by the CARNMT1 gene (also known as the UPF0586 gene) (Kwiatkowski et al., 2018). Although the HNMT and HNMT-like genes are distinct, HNMT-like is presumably the result of gene duplication with a novel enzymatic activity (Drozak et al., 2013; Kwiatkowski et al., 2018). Our results were consistent with previous reports that the HNMT and HNMT-like genes are located in direct proximity on chromosome 7, near the positions of other genes (e.g., THSD7B, SPOPL, and NXPH2) in most vertebrates (Kwiatkowski et al., 2018).

Current research identified candidate gene involved in the process of converting carnosine to anserine. It means that those genetic markers will be useful to control the ratio between anserine and carnosine. It is meaningful because there are synergistic effects of anserine and carnosine on taste, reducing the bitterness of sole carnosine and increasing umami (Kajiya et al., 2023). Although potential candidate genes were identified, causal SNPs related to the traits were not detected in these genes. Therefore, functional studies exploring SNPs in the identified genes are needed to confirm their effects on the anserine and carnosine contents in chickens.

CONCLUSIONS

Anserine and carnosine in meat have health benefits for humans, and their contents can be improved through breeding. Through GWAS, the present investigation identified HNMT and HNMT-like as candidate genes related to the anserine and carnosine contents in chicken breast meat. The HNMT-like gene encodes the enzyme involved in anserine synthesis in chicken muscles. And the HNMT gene is involved in the histidine metabolism which is a precursor of anserine. The present study yielded key insights regarding the genetic basis for anserine and carnosine as bioactive compounds; the findings provide a foundation for marker-assisted selection to improve the flavor of chicken meat to satisfy future consumer demands.

DISCLOSURES

The authors declare no conflicts of interest.

ACKNOWLEDGMENTS

This research was funded by the Rural Development Administration, South Korea (grant number RS-2021-RD010125 [PJ016205]).

Footnotes

Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2024.103590.

Appendix. Supplementary materials

mmc1.docx (276.1KB, docx)
mmc2.zip (4.4MB, zip)

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