[논문]Genome-wide association studies on collagen contents trait for meat quality in Hanwoo

KyeongHye Won; Dohyun Kim; Inho Hwang; Hak-Kyo Lee; Jae-Don Oh

doi:10.5187/jast.2022.e110

Genome-wide association studies on collagen contents trait for meat quality in Hanwoo 원문보기

Journal of animal science and technology : JAST, v.65 no.2, 2023년, pp.311 - 323

KyeongHye Won (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) , Dohyun Kim (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) , Inho Hwang (Department of Animal Science, Jeonbuk National University) , Hak-Kyo Lee (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) , Jae-Don Oh (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University)

Abstract ▼ AI-Helper

Beef consumers valued meat quality traits such as texture, tenderness, juiciness, flavor, and meat color that determining consumers' purchasing decision. Most research on meat quality has focused on marbling, a key characteristic related to meat eating quality. However, other important traits such as meat texture, tenderness, and color have not much studied in cattle. Among these traits, meat tenderness and texture of cattle are among the most important factors affecting quality evaluation of consumers. Collagen is the main component of connective tissues.It greatly affects meat tenderness. The objective of this study was to determine significant variants and candidate genes associated with collagen contents trait (total collagen) through genome-wide association studies (GWAS). Phenotypic and genomic data from 135 Hanwoo were used. The BLUPF90 family program and GRAMMAR method for GWAS were applied in this study. A total of 73 potential single nucleotide polymorphisms (SNPs) showed significant associations with collagen content. They were located in or near 108 candidate genes. TMEM135 and ME3 genes were identified to have the most significant SNPs associated with collagen contents trait. Data indicated that these genes were related to collagen. Biological processes and pathways for the prediction of biological functions of candidate genes were confirmed. We found that candidate genes were involved in positive regulation of CREB transcription factor activity and actin cytoskeleton related to tenderness and texture of beef. Three genes (CRTC3, MYO1C and MYLK4) belonging to these biological functions were related to tenderness. These results provide a basis for improving genomic characteristics of Hanwoo for the production of tender beef. Furthermore, they could be used they could be used as an index to select desired traits for consumers.

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표/그림 (11)

그림 Fig. 1. Flow chart related to GWAS analysis using genomic and phenotypic data. IBS, identity by state; QC, quality control; GWAS, genome-wide association studies; GWAS, genome-wide association studies; SNPs, single nucleotide polymorphisms; QQ, quantile-quantile.
표 Table 1. The basic statistics for phenotypic data
표 Table 2. The number of available SNPs and average interval distance between adjacent SNPs in Bovine SNP50k chip
그림 Fig. 2. The QQ-plot for the studied total collagen contents trait. The dotted line represents the 95% concentration band under the null hypothesis no association between trait and SNPs. The green dots represent the p-values. QQ, quantile-quantile; SNPs, single nucleotide polymorphisms.
표 Table 3. The basic statistics for results of BLUPF90 analysis
그림 Fig. 3. The Manhattan plot of SNP effects for GWAS analysis using GRAMMAR methods in PLINK. SNP, single nucleotide polymorphism; GWAS, genome-wide association studies.
그림 Fig. 4. The Manhattan plot of GWAS for total collagen contents trait with significance thresholds indicated at -log₁₀P > 1 × 10^-3. The orange dots represent significant SNPs associated with total collagen contents trait. GWAS, genome-wide association studies; SNPs, single nucleotide polymorphisms.
표 Table 4. Signifcant SNPs (total collagen)
표 Table 4. Continued
표 Table 5. The results of gene ontology (GO) analysis of candidate genes associated with total collagen contents trait from GWAS analysis
표 Table 6. The results of KEGG pathway analysis of candidate genes associated with total collagen contents trait from GWAS analysis

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문제 정의

Thus, the objective of this study was to detect significant variants and candidate genes associated with collagen contents trait (total collagen) using GWAS. Furthermore, this study will ultimately contribute to the the production of tender beef with short feeding periods.

성능/효과

4 and Table 4). A total of 108 candidate genes associated with significant SNPs were annotated based on Bos taurus genome. The most significant SNP was confirmed to be UA-IFASA-8514 (chr29:8936383) in Transmembrane protein 135 (TMEM135) and Malic Enzyme 3 (ME3) genes.
We identified the number of SNPs considered useful for Hanwoo per chromosome, ranging from a minimum of 799 to a maximum of 2,909. About 89.1% of total SNPs were selected as available SNPs. The average distance of adjacent SNPs for each chromosome was 54.
Based on p < 0.001, a total of 73 SNPs were significantly associated with the trait (Fig
001. Candidate genes associated with significant SNPs were annotated within 500 kb downstream and upstream of detected SNPs based on the Bos taurus transfer format (GTF) (version ARS-UCD1.2.104) in Ensembl database.
We identified functions of candidate genes associated with total collagen contents trait from GO and KEGG analysis using DAVID (Tables 5 and 6). In biological process from GO, we confirmed eight gene ontologies: negative regulation of peptidyl-serine dephosphorylation (GO:1902309), negative regulation of ubiquitin-protein transferase activity (GO:0051444), receptor localization to synapse (GO:0097120), T cell receptor signaling pathway (GO:0050852), negative regulation of epidermal growth factor-activated receptor activity (GO:0007175), somite development (GO:0061053), positive regulation of CREB transcription factor activity (GO:0032793), and amino acid transmembrane transport (GO:0003333). In cellular component, we identified seven gene ontologies: cytosol (GO:0005829), nucleoplasm (GO:0005654), actin cytoskeleton (GO:0015629), perinuclear region of cytoplasm (GO:0048471), cytoplasm (GO:0005737), nuclear speck (GO:0016607), and cell projection (GO:0042995).
1% of total SNPs were selected as available SNPs. The average distance of adjacent SNPs for each chromosome was 54.343 kb (Table 2).
We identified basic statistics for phenotypic data of 129 Hanwoo after QC. The estimates for collagen contents traits were on average 0.362, 0.250 and 0.114 respectively (Table 1).
A total of 108 candidate genes associated with significant SNPs were annotated based on Bos taurus genome. The most significant SNP was confirmed to be UA-IFASA-8514 (chr29:8936383) in Transmembrane protein 135 (TMEM135) and Malic Enzyme 3 (ME3) genes.
Through the QC test, 5,715 SNPs out of 52,195 SNPs were removed and 46,480 SNPs associated with collagen contents trait were finally used for GWAS analysis. We confirmed the difference in the number of available SNPs per chromosome and the interval size (kb) of each autosome of autosuomes 1 to 29 before and after QC.
Through the QC test, 5,715 SNPs out of 52,195 SNPs were removed and 46,480 SNPs associated with collagen contents trait were finally used for GWAS analysis. We confirmed the difference in the number of available SNPs per chromosome and the interval size (kb) of each autosome of autosuomes 1 to 29 before and after QC. We identified the number of SNPs considered useful for Hanwoo per chromosome, ranging from a minimum of 799 to a maximum of 2,909.
We identified 129 individuals after removing six (ID: 002311515862, 002311652670, 002300057089, 002085007947, 002114973907 and 002112336318) out of 135 individuals by IBS distance test and outlier. We identified basic statistics for phenotypic data of 129 Hanwoo after QC.
We confirmed the difference in the number of available SNPs per chromosome and the interval size (kb) of each autosome of autosuomes 1 to 29 before and after QC. We identified the number of SNPs considered useful for Hanwoo per chromosome, ranging from a minimum of 799 to a maximum of 2,909. About 89.

후속연구

Variants and genes identified in this study are expected to provide important information for genomic selection of phenotypes to improve meat quality of Hanwoo. Furthermore, they provide a basis for further studies on consumption traits.
Thus, the objective of this study was to detect significant variants and candidate genes associated with collagen contents trait (total collagen) using GWAS. Furthermore, this study will ultimately contribute to the the production of tender beef with short feeding periods.
This causes production of a large amount of methane gas that contributes to global warming, which is also related to the environment. Therefore, it is necessary to produce tender beef with a short-term of breeding.
Variants and genes identified in this study are expected to provide important information for genomic selection of phenotypes to improve meat quality of Hanwoo. Furthermore, they provide a basis for further studies on consumption traits.

참고문헌 (38)

Bulik-Sullivan BK, Loh PR, Finucane HK, Ripke S, Yang J, Schizophrenia Working Group？of the Psychiatric Genomics Consortium, et al. LD score regression distinguishes confounding？from polygenicity in genome-wide association studies. Nat Genet. 2015;47:291-5. https://doi.org/10.1038/ng.3211

상세보기
Strucken EM, Al-Mamun HA, Esquivelzeta-Rabell C, Gondro C, Mwai OA, Gibson JP.？Genetic tests for estimating dairy breed proportion and parentage assignment in East African？crossbred cattle. Genet Sel Evol. 2017;49:67. https://doi.org/10.1186/s12711-017-0342-1

상세보기
O'Quinn TG, Legako JF, Brooks JC, Miller MF. Evaluation of the contribution of tenderness,？juiciness, and flavor to the overall consumer beef eating experience. Transl Anim Sci. 2018;2:26-36. https://doi.org/10.1093/tas/txx008

상세보기
Liu J, Ellies-Oury MP, Stoyanchev T, Hocquette JF. Consumer perception of beef quality and？how to control, improve and predict it? Focus on eating quality. Foods. 2022;11:1732. https://doi.org/10.3390/foods11121732

상세보기
Bedhane M, van der Werf J, Gondro C, Duijvesteijn N, Lim D, Park B, et al. Genome-wide？association study of meat quality traits in Hanwoo beef cattle using imputed whole-genome？sequence data. Front Genet. 2019;10:1235. https://doi.org/10.3389/fgene.2019.01235

상세보기
McCormick RJ. Extracellular modifications to muscle collagen: implications for meat quality.？Poult Sci. 1999;78:785-91. https://doi.org/10.1093/ps/78.5.785

상세보기
Zhu Y, Gagaoua M, Mullen AM, Kelly AL, Sweeney T, Cafferky J, et al. A proteomic study？for the discovery of beef tenderness biomarkers and prediction of Warner-Bratzler shear force？measured on longissimus thoracis muscles of young Limousin-Sired bulls. Foods. 2021;10:952.？https://doi.org/10.3390/foods10050952

상세보기
Lepetit J. Collagen contribution to meat toughness: theoretical aspects. Meat Sci. 2008;80:960-7. https://doi.org/10.1016/j.meatsci.2008.06.016

상세보기
Bernard C, Cassar-Malek I, Le Cunff M, Dubroeucq H, Renand G, Hocquette JF. New？indicators of beef sensory quality revealed by expression of specific genes. J Agric Food Chem.？2007;55:5229-37. https://doi.org/10.1021/jf063372l

상세보기
Maltin C, Balcerzak D, Tilley R, Delday M. Determinants of meat quality: tenderness. Proc？Nutr Soc. 2003;62:337-47. https://doi.org/10.1079/PNS2003248

상세보기
Mullen AM, Stapleton PC, Corcoran D, Hamill RM, White A. Understanding meat quality？through the application of genomic and proteomic approaches. Meat Sci. 2006;74:3-16.？https://doi.org/10.1016/j.meatsci.2006.04.015

상세보기
Taye M, Kim J, Yoon SH, Lee W, Hanotte O, Dessie T, et al. Whole genome scan reveals the？genetic signature of African Ankole cattle breed and potential for higher quality beef. BMC？Genet. 2017;18:11. https://doi.org/10.1186/s12863-016-0467-1

상세보기
Meuwissen THE, Hayes BJ, Goddard ME. Prediction of total genetic value using genome-wide？dense marker maps. Genetics. 2001;157:1819-29. https://doi.org/10.1093/genetics/157.4.1819

상세보기
Goddard ME, Hayes BJ. Mapping genes for complex traits in domestic animals and their use？in breeding programmes. Nat Rev Genet. 2009;10:381-91. https://doi.org/10.1038/nrg2575

상세보기
Lee SH, Kim CN, Ko KB, Park SP, Kim HK, Kim JM, et al. Comparisons of beef fatty acid？and amino acid characteristics between Jeju black cattle, Hanwoo, and Wagyu breeds. Food Sci？Anim Resour. 2019;39:402-9. https://doi.org/10.5851/kosfa.2019.e33

원문보기 상세보기
Kolar K. Colorimetric determination of hydroxyproline as measure of collagen content in meat and？meat products: NMKL collaborative study. J Assoc Off Anal Chem. 1990;73:54-7. https://doi.org/10.1093/jaoac/73.1.54
Hill F. The solubility of intramuscular collagen in meat animals of various ages. J Food Sci.？1966;31:161-6. https://doi.org/10.1111/j.1365-2621.1966.tb00472.x

상세보기
Kim YA, Van Ba H, Dashdorj D, Hwang I. Effect of high-pressure processing on the quality？characteristics and shelf-life stability of Hanwoo beef marinated with various sauces. Korean J？Food Sci Anim Resour. 2018;38:679-92. https://doi.org/10.5851%2Fkosfa.2018.e4

원문보기 상세보기
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: a tool？set for whole-genome association and population-based linkage analyses. Am J Hum Genet.？2007;81:559-75. https://doi.org/10.1086/519795

상세보기
Hammami H, Rekik B, Soyeurt H, Bastin C, Bay E, Stoll J, et al. Accessing genotype by？environment interaction using within- and across-country test-day random regression sire？models. J Anim Breed Genet. 2009;126:366-77.

상세보기
VanRaden PM. Efficient methods to compute genomic predictions. J Dairy Sci. 2008;91:4414-23. https://doi.org/10.3168/jds.2007-0980

상세보기
Srivastava S, Lopez BI, de las Heras-Saldana S, Park JE, Shin DH, Chai HH, et al. Estimation of genetic parameters by single-trait and multi-trait models for carcass traits in Hanwoo cattle.？Animals. 2019;9:1061. https://doi.org/10.3390/ani9121061

상세보기
Aulchenko YS, de Koning DJ, Haley C. Genomewide rapid association using mixed model？and regression: a fast and simple method for genomewide pedigree-based quantitative trait loci？association analysis. Genetics. 2007;177:577-85. https://doi.org/10.1534/genetics.107.075614

상세보기
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool？for the unification of biology. Nat Genet. 2000;25:25-9. https://doi.org/10.1038/75556

상세보기
Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids？Res. 2000;28:27-30. https://doi.org/10.1093/nar/28.1.27

상세보기
Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, et al. DAVID: a web server for？functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic？Acids Res. 2022;50:W216-21. https://doi.org/10.1093/nar/gkac194

상세보기
Weston AR, Rogers RW, Althen TG. Review: the role of collagen in meat tenderness. Prof？Anim Sci. 2002;18:107-11. https://doi.org/10.15232/S1080-7446(15)31497-2

상세보기
Belbin GM, Odgis J, Sorokin EP, Yee MC, Kohli S, Glicksberg BS, et al. Genetic identification？of a common collagen disease in puerto ricans via identity-by-descent mapping in a health？system. eLife. 2017;6:e25060. https://doi.org/10.7554/eLife.25060

상세보기
Zhang Z, Bai M, Barbosa GO, Chen A, Wei Y, Luo S, et al. Broadly conserved roles of？TMEM131 family proteins in intracellular collagen assembly and secretory cargo trafficking.？Sci Adv. 2020;6:eaay7667. https://doi.org/10.1126/sciadv.aay7667

상세보기
Beasley HK, Rodman TA, Collins GV, Hinton A Jr, Exil V. TMEM135 is a novel regulator of？mitochondrial dynamics and physiology with implications for human health conditions. Cells.？2021;10:1750. https://doi.org/10.3390/cells10071750

상세보기
McDonough JE, Kaminski N, Thienpont B, Hogg JC, Vanaudenaerde BM, Wuyts WA. Gene？correlation network analysis to identify regulatory factors in idiopathic pulmonary fibrosis.？Thorax. 2019;74:132-40. https://doi.org/10.1136/thoraxjnl-2018-211929

상세보기
Phelps KJ, Johnson DD, Elzo MA, Paulk CB, Gonzalez JM. Effect of Brahman genetics？on myofibrillar protein degradation, collagen crosslinking, and tenderness of the longissimus？lumborum. J Anim Sci. 2017;95:5397-406. https://doi.org/10.2527/jas2017.2022

상세보기
Liu J, Wang L, Chen W, Li J, Shan T. CRTC3 regulates the lipid metabolism and adipogenic？differentiation of porcine intramuscular and subcutaneous adipocytes by activating the calcium？pathway. J Agric Food Chem. 2021;69:7243-55. https://doi.org/10.1021/acs.jafc.1c02021

상세보기
Thompson JM. The effects of marbling on flavour and juiciness scores of cooked beef, after adjusting？to a constant tenderness. Aust J Exp Agric. 2004;44:645-52. https://doi.org/10.1071/EA02171

상세보기
Nian Y, Moloney AP, Li C, Allen P, Harrison SM, Prendiville R, et al. A comparison of meat？composition, tenderness and the fatty acid profile of three muscles from Holstein-Friesian bulls？from production system resulting in final ages of either < 16 or 19 months. Anim Prod Sci.？2022;62:368-80. https://doi.org/10.1071/AN20697

상세보기
Cui HX, Liu RR, Zhao GP, Zheng MQ, Chen JL, Wen J. Identification of differentially expressed？genes and pathways for intramuscular fat deposition in pectoralis major tissues of fast-and slow-growing chickens. BMC Genomics. 2012;13:213. https://doi.org/10.1186/1471-2164-13-213

상세보기
Zhao C, Ji G, Carrillo JA, Li Y, Tian F, Baldwin RL, et al. The profiling of DNA methylation？and its regulation on divergent tenderness in Angus beef cattle. Front Genet. 2020;11:939.？https://doi.org/10.3389/fgene.2020.00939

상세보기
Yang Y, Yang J, Ma J, Yu Q, Han L. iTRAQ-mediated analysis of the relationship between？proteomic changes and yak longissimus lumborum tenderness over the course of postmortem？storage. Sci Rep. 2021;11:10450. https://doi.org/10.1038/s41598-021-90012-0

상세보기

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