基因组和DNA甲基化组联合分析筛选猪肉质性状关键基因

doi:10.3864/j.issn.0578-1752.2024.07.014

中国农业科学 ›› 2024, Vol. 57 ›› Issue (7): 1394-1406.doi: 10.3864/j.issn.0578-1752.2024.07.014

基因组和DNA甲基化组联合分析筛选猪肉质性状关键基因

赵真坚(), 王凯, 陈栋, 申琦, 余杨, 崔晟頔, 王俊戈, 陈子旸, 禹世欣, 陈佳苗, 王翔枫, 唐国庆()

四川农业大学动物科技学院/农业农村部畜禽生物组学重点实验室/畜禽遗传资源发掘与创新利用四川省重点实验室/猪禽种业全国重点实验室，成都 611130

收稿日期:2023-10-18 接受日期:2023-12-31 出版日期:2024-04-01 发布日期:2024-04-09
通信作者:
唐国庆，E-mail：tyq003@163.com
联系方式: 赵真坚，E-mail：530773281@qq.com。
基金资助:
四川省科技厅项目(2020YFN0024); 四川省科技厅项目(2021ZDZX0008); 四川省科技厅项目(2021YFYZ0030); 四川省猪创新团队项目(sccxtd-2022-08)

Integrated Aanalysis of Genome and DNA Methylation for Screening Key Genes Related to Pork Quality Traits

ZHAO ZhenJian(), WANG Kai, CHEN Dong, SHEN Qi, YU Yang, CUI ShengDi, WANG JunGe, CHEN ZiYang, YU ShiXin, CHEN JiaMiao, WANG XiangFeng, TANG GuoQing()

College of Animal Science and Technology, Sichuan Agricultural University/Key Laboratory of Livestock and Poultry Multi-Omics, Ministry of Agriculture and Rural Affairs/Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province/State Key Laboratory of Swine and Poultry Breeding Industry, Chengdu 611130

Received:2023-10-18 Accepted:2023-12-31 Published:2024-04-01 Online:2024-04-09

摘要/Abstract

摘要：

【背景】猪的肉质性状是重要的经济性状。研究影响各类肉质性状的分子机制，发掘关键基因，从而指导猪的遗传改良，对改善猪肉品质具有重要意义。当前肉质相关的机制研究主要是基于DNA的基因组研究，而对肉质性状的DNA甲基化研究以及结合基因组和甲基化组的综合分析却鲜有报道。【目的】通过基因组和DNA甲基化组联合分析，筛选、鉴定了影响猪肉质的潜在关键基因。为猪肉品质的遗传改良研究提供借鉴。【方法】检测了140头大白猪背最长肌的28个肉质性状，通过表观基因组关联分析（EWAS）与全基因组关联分析（GWAS）筛选了各性状显著关联的CpG和SNP位点。随后以SNP为协变量对GWAS和EWAS重叠的显著关联位点进行条件关联分析，进一步筛选具有独立效应的CpG位点。然后以CpG位点的甲基化水平为因变量，以SNP为自变量进行关联分析从而鉴定甲基化数量性状位点（meQTL）。最后使用顺式甲基化数量性状位点（cis-meQTL）作为工具变量进行孟德尔随机化分析，从而推断cis-meQTL与表型之间的因果关系，同时对位点进行注释，鉴定潜在的关键基因。【结果】（1）在屠宰45 min黄度值（b_45min）、滴水损失（DL）、二十二碳六烯酸（C22:6n-3）3个肉质性状上，EWAS和GWAS在相同基因组区域鉴定到显著关联位点。（2）b_45min的7个CpG位点在条件关联分析后仍保持显著，DL有1个CpG位点在条件关联分析后仍保持显著，而C22:6n-3的3个位点在使用SNP作为协变量分析后不再显著，表明EWAS鉴定的b_45min的7个CpG位点和DL的1个CpG位点的显著关联不受附近的显著SNP影响。（3）b_45min的7个CpG位点和DL的1个CpG位点共鉴定了10个meQTL，但绝大多数是trans-meQTL，只有一个CpG位点（SSC12:44 254 675 bp）鉴定到一个cis-meQTL，表明该位点可能受到近距离SNP调控。（4）孟德尔随机化分析显示该CpG位点（SSC12:44 254 675 bp）与b_45min表型存在一定的因果关联。（5）对该位点注释发现，距离CpG位点（SSC12:44 254 675 bp）和其cis-meQTL最近的基因是NOS2，且CpG位点位于NOS2基因内。【结论】综合DNA甲基化组合基因组数据联合分析结果，可以推测NOS2基因是肉色性状关键候选基因，其DNA甲基化、SNP共同作用调控基因表达，进而影响肉色性状相关基因表达。

关键词: 表观基因组关联分析, 全基因组关联分析, 肉质性状, DNA甲基化, 甲基化数量性状位点

Abstract:

【Background】 The meat quality traits of pigs are important economic traits. Studying the molecular mechanisms that affect various meat quality traits and discovering key genes can guide genetic improvement of pigs and have significant implications for improving pork quality. Currently, those researches on meat-related mechanisms were mainly based on DNA genomics, while studies on DNA methylation related to meat quality traits, as well as integrated analysis of combining genomics and methylation, are scarce. 【Objective】 The potential key genes affecting pork meat quality were screened and identified by combined analysis of genome and DNA methylome, so as to provide a reference for the genetic improvement of pork quality. 【Method】 In this study, 28 meat quality traits of the ongissimus dorsi muscle of 140 Large White pigs were examined. Epigenome-wide association analysis (EWAS) and genome-wide association analysis (GWAS) were performed to identify CpG and SNP sites significantly associated with each trait. Subsequently, the conditional association analysis was performed by using SNPs as covariates on the significantly associated sites overlapping between GWAS and EWAS to further identify CpG sites with independent effects. Association analysis was then conducted to identify methylation quantitative trait loci (meQTL) by using the methylation levels of CpG sites as the dependent variable and SNPs as the independent variable. Finally, the cis-methylation quantitative trait loci (cis-meQTL) were used as instrumental variables for Mendelian randomization analysis to infer the causal relationship between cis-meQTL and phenotypes, while potential key genes at the loci were annotated and identified. 【Result】 (1) The significant associated sites were identified in the same genomic regions for the meat quality traits, namely yellowness value at slaughter 45 minutes postmortem (b_45min), drip loss (DL), and docosahexaenoic acid (C22:6n-3), by both EWAS and GWAS. (2) After conditional association analysis, seven CpG sites for b_45min and one CpG site for DL remained significant, while the three sites for C22:6n-3 were no longer significant after using SNPs as covariates, indicating that the significant associations of the seven CpG sites for b_45min and one CpG site for DL identified by EWAS were not influenced by nearby significant SNPs. (3) A total of ten meQTL were identified for the seven CpG sites for b_45min and one CpG site for DL, but the majority were trans-meQTL, with only one CpG site (SSC12:44 254 675 bp) identifying a cis-meQTL, suggesting that this site might be regulated by nearby SNPs. (4) Mendelian randomization analysis showed a causal relationship between the CpG site (SSC12:44 254 675 bp) and the b_45min phenotype. (5) annotation of the locus revealed that the nearest gene to the CpG site (SSC12:44 254 675 bp) and its cis-meQTL was NOS2, and the CpG site was located within the NOS2 gene. 【Conclusion】 Based on the integrated analysis of DNA methylation and genomics data, this study proposed that the NOS2 gene might be a key candidate gene for meat color traits. DNA methylation and SNP jointly regulated gene expression, thereby affecting the expression of genes related to meat color traits.

Key words: epigenome-wide association study (EWAS), genome-wide association study (GWAS), meat quality traits, DNA methylation, meQTL

赵真坚, 王凯, 陈栋, 申琦, 余杨, 崔晟頔, 王俊戈, 陈子旸, 禹世欣, 陈佳苗, 王翔枫, 唐国庆. 基因组和DNA甲基化组联合分析筛选猪肉质性状关键基因[J]. 中国农业科学, 2024, 57(7): 1394-1406.

ZHAO ZhenJian, WANG Kai, CHEN Dong, SHEN Qi, YU Yang, CUI ShengDi, WANG JunGe, CHEN ZiYang, YU ShiXin, CHEN JiaMiao, WANG XiangFeng, TANG GuoQing. Integrated Aanalysis of Genome and DNA Methylation for Screening Key Genes Related to Pork Quality Traits[J]. Scientia Agricultura Sinica, 2024, 57(7): 1394-1406.

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性状 Trait	GWAS关联 GWAS associations		EWAS关联 EWAS associations
性状 Trait	染色体SSC	位点或区域 Position or Region (bp)	SNP数量 Number of SNP	CpG位点 CpG site (bp)
b_45min	1	4049232	1	SSC1:4667485
b_45min	6	5191168-5483926	10	SSC6:4737404
b_45min	7	9770008-10877899	20	SSC7:10489621
b_45min	10	35692369	1	SSC10:36329538
b_45min	12	44218560	1	SSC12:44254675
b_45min	14	17744509-18820911	19	SSC14:17859513
b_45min	18	49231979-50010893	7	SSC18:48429425
b_45min	18	49231979-50010893	7	SSC18:50979305
DL	7	121791317	1	SSC7:120954182
C22:6n-3	4	101860069-103765886	146	SSC4:102796889
C22:6n-3	4	101860069-103765886	146	SSC4:103218200
C22:6n-3	4	101860069-103765886	146	SSC4:103552805

性状Trait	CpG位点 CpG site (bp)	染色体SSC	位置 Position (bp)	P value (EWAS)	P value (after correct)
b_45min	SSC1: 4667485	1	4667485	3.95E-9	3.95E-9
	SSC6: 4737404	6	4737404	7.59E-9	0.35
	SSC7: 10489621	7	10489621	1.53E-9	1.53E-9
	SSC10: 36329538	10	36329538	2.76E-13	2.76E-13
	SSC12: 44254675	12	44254675	5.45E-9	5.45E-9
	SSC14: 17859513	14	17859513	1.26E-9	1.26E-9
	SSC18: 48429425	18	48429425	1.06E-10	1.06E-10
	SSC18: 50979305	18	50979305	1.18E-9	1.18E-9
DL	SSC7: 120954182	7	120954182	7.79E-9	7.79E-9
C22:6n-3	SSC4: 102796889	4	102796889	1.32E-12	0.99
	SSC4: 103218200	4	103218200	3.32E-9	0.13
	SSC4: 103552805	4	103552805	1.32E-12	0.99

CpG位点 CpG site (bp)	甲基化数量性状位点 meQTL	顺式meQTL cis-meQTL	反式meQTL trans-meQTL	SNP
SSC1:4667485	0	0	0	0
SSC7:10489621	2	0	2	9
SSC10:36329538	0	0	0	0
SSC12:44254675	2	1	1	11
SSC14:17859513	2	0	2	46
SSC18:48429425	0	0	0	0
SSC18:50979305	3	0	3	345
SSC7:120954182	1	0	1	4

基因组和DNA甲基化组联合分析筛选猪肉质性状关键基因

Integrated Aanalysis of Genome and DNA Methylation for Screening Key Genes Related to Pork Quality Traits

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