联合GWAS和转录组分析挖掘与白斑狗鱼耐高温性状关联的SNP

doi:10.19586/j.2095-2341.2024.0184

生物技术进展 ›› 2025, Vol. 15 ›› Issue (3): 432-445.DOI: 10.19586/j.2095-2341.2024.0184

联合GWAS和转录组分析挖掘与白斑狗鱼耐高温性状关联的SNP

海萨·艾也力汗null¹(), 焦飞¹, 刘鸿¹, 呼德拉提·阿那斯null¹, 沈玉帮²()

^1.新疆维吾尔自治区水产科学研究所，乌鲁木齐 830000
^2.上海海洋大学水产与生命学院，上海 201306

收稿日期:2024-11-24 接受日期:2025-02-17 出版日期:2025-05-25 发布日期:2025-07-01
通讯作者: 沈玉帮
作者简介:海萨·艾也力汗 E-mail：hbahjan@126.com；
基金资助:
国家自然科学基金项目(32060826)

Integrating GWAS and Transcriptome Profiling to Identify SNP Markers Linked to High-temperature Tolerance in Esox lucius

AYELHAN·Haysa¹(), Fei JIAO¹, Hong LIU¹, ANASI·Hudelati¹, Yubang SHEN²()

^1.Xinjiang Fishery Research Institute, Urumqi 830000, China
^2.College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China

Received:2024-11-24 Accepted:2025-02-17 Online:2025-05-25 Published:2025-07-01
Contact: Yubang SHEN

摘要/Abstract

摘要：

研究旨在提升白斑狗鱼对极端高温的适应能力和满足向南部温暖地区养殖发展的需求，进一步发掘与其耐高温性状显著关联的基因位点和候选基因。首先基于前期对热敏感与耐高温群体的简化基因组测序数据，利用混合线性模型（mixed-linear model， MLM）进行全基因组关联分析（genome-wide association study， GWAS）筛选出与耐高温性状显著关联的单核苷酸多态性(single nucleotide polymorphism， SNP）位点；继而采用转录组测序技术对4组不同热处理幼鱼的脑组织进行基因差异表达分析；随后联合GWAS和转录组分析筛选出候选基因和SNP位点；最后利用Sanger测序技术，以耐高温组和参考组为材料，对显著关联的SNP位点加以验证。结果显示，GWAS分析获得了471个与耐高温性状显著关联的SNP位点。GO和KEGG分析显示，DEGs显著富集于内质网应激和免疫系统相关通路。GSEA分析显示，热胁迫84 h后先天免疫反应被激活，并且与NAD(+)ADP-核糖基转移酶活性相关的基因被诱导。先天免疫反应启动和调控相关基因的PPI分析显示，parp14、parp9、stat1和stat3是核心基因，同时也是互作基因。热应激反应中parp14可能通过调控stat1、stat3等下游效应基因来发挥保护细胞的作用。GWAS获得的SNP位点中，有2个SNP位点位于parp14基因的第三外显子。验证结果显示，parp14基因第三外显子中的2个SNP位点与耐高温性状显著相关，且为完全连锁不平衡，其中位点rsc.646T>C为错义突变，位点rsc.777G>A为同义突变。研究筛选出与白斑狗鱼耐高温相关的候选基因及与耐高温性状显著关联的2个SNP位点，可为白斑狗鱼耐高温性状的遗传机制和分子标记辅助育种提供理论依据。

关键词: 白斑狗鱼, 耐高温性状, GWAS, 转录组, parp14, SNP

Abstract:

To enhance the extreme high-temperature adaptability of Esox lucius for aquaculture expansion to southern warm regions and identify genetic loci associated with thermal tolerance， we integrated genome-wide association study （GWAS） and transcriptome analysis. Using reduced-representation genome sequencing data from heat-sensitive and heat-tolerant populations， GWAS analysis with an MLM model identified 471 SNPs significantly associated with thermal tolerance traits. Concurrently， transcriptome sequencing of juvenile brain tissues exposed to varying heat stress durations revealed differential gene expression patterns. Functional enrichment analyses demonstrated significant enrichment of differentially expressed genes （DEGs） in endoplasmic reticulum stress and immune-related pathways. GSEA analysis indicated activation of innate immune responses at 84 h of heat stress， with specific induction of NAD（+） ADP-ribosyltransferase activity-related genes. Protein-protein interaction （PPI） network analysis identified parp14， parp9， stat1， and stat3 as core regulators of innate immune responses. Notably， two GWAS-derived SNPs located in exon 3 of the parp14 gene—rsc.646T>C （missense mutation） and rsc.777G>A （synonymous mutation）—exhibited complete linkage disequilibrium and were significantly correlated with thermal tolerance traits. Sanger sequencing validation in heat-stressed and reference populations confirmed these associations. Our findings reveal candidate genes and functional SNP markers for high-temperature tolerance in E. lucius， providing insights into its genetic mechanisms and supporting marker-assisted breeding strategies.

Key words: Esox lucius, high temperature tolerance, GWAS, transcriptome, parp14, SNP

中图分类号:

Q789

海萨·艾也力汗null, 焦飞, 刘鸿, 呼德拉提·阿那斯null, 沈玉帮. 联合GWAS和转录组分析挖掘与白斑狗鱼耐高温性状关联的SNP[J]. 生物技术进展, 2025, 15(3): 432-445.

AYELHAN·Haysa, Fei JIAO, Hong LIU, ANASI·Hudelati, Yubang SHEN. Integrating GWAS and Transcriptome Profiling to Identify SNP Markers Linked to High-temperature Tolerance in Esox lucius[J]. Current Biotechnology, 2025, 15(3): 432-445.

图/表 11

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基因名称	引物名称	引物序列(5'→3')	退火温度T_m/℃	目的
parp14	PARP14 DF1 PARP14DR1	5′-ACACTGCTCTGACATCGGAC-3′ 5′-CCTTTAGGTAGCGCAGGAGG-3′	60	荧光定量PCR
parp9	PARP9 DF23 PARP9 DR2	5′-TGGAGGTCTTGCACTAGCAC-3′ 5′-ACTGTATGTCTGTTTTCAACCTTC-3′	60	荧光定量PCR
stat1	STAT1a DF1 STAT1a DR1	5′-GAGGACCCCATTCACATGGC-3′ 5′-GTATGCTTCTGGCAACAGCC-3′	60	荧光定量PCR
stat3	STAT3 DF1 STAT3 DR1	5′-AGCCAACAAAGAGTCCCACG-3′ 5′-TACGCCGTAGGTTATGCTGG-3′	60	荧光定量PCR
β-actin	β-actin F1 β-actin R1	5′-CAGAGCAAGAGAGGTATC-3′ 5′-GTTGTAGAAGGTGTGATG-3′	60	荧光定量PCR
hsp90α	HSP90αF2 HSP90αR2	5′-GGCTGAGATTGCCCAGTTGA-3′ 5′-TTGCTAGGGTCTGTCAAGCTC-3′	60	荧光定量PCR
hspa4	HSPA4F1 HSPA4R1	5′-GCGACCGAAGTACACCATCA-3′ 5′-AAGCCCTGCCATGGAATCTC-3′	60	荧光定量PCR
parp14	7125CXF2 7125CXR2	5′-ACTGTTTGAACAGCTCGTGGA-3′ 5′-GACCCCTAGATCCACCTGTACTT-3′	60	SNP验证

基因名称	引物名称	引物序列(5'→3')	退火温度T_m/℃	目的
parp14	PARP14 DF1 PARP14DR1	5′-ACACTGCTCTGACATCGGAC-3′ 5′-CCTTTAGGTAGCGCAGGAGG-3′	60	荧光定量PCR
parp9	PARP9 DF23 PARP9 DR2	5′-TGGAGGTCTTGCACTAGCAC-3′ 5′-ACTGTATGTCTGTTTTCAACCTTC-3′	60	荧光定量PCR
stat1	STAT1a DF1 STAT1a DR1	5′-GAGGACCCCATTCACATGGC-3′ 5′-GTATGCTTCTGGCAACAGCC-3′	60	荧光定量PCR
stat3	STAT3 DF1 STAT3 DR1	5′-AGCCAACAAAGAGTCCCACG-3′ 5′-TACGCCGTAGGTTATGCTGG-3′	60	荧光定量PCR
β-actin	β-actin F1 β-actin R1	5′-CAGAGCAAGAGAGGTATC-3′ 5′-GTTGTAGAAGGTGTGATG-3′	60	荧光定量PCR
hsp90α	HSP90αF2 HSP90αR2	5′-GGCTGAGATTGCCCAGTTGA-3′ 5′-TTGCTAGGGTCTGTCAAGCTC-3′	60	荧光定量PCR
hspa4	HSPA4F1 HSPA4R1	5′-GCGACCGAAGTACACCATCA-3′ 5′-AAGCCCTGCCATGGAATCTC-3′	60	荧光定量PCR
parp14	7125CXF2 7125CXR2	5′-ACTGTTTGAACAGCTCGTGGA-3′ 5′-GACCCCTAGATCCACCTGTACTT-3′	60	SNP验证

染色体	SNP数量	-lg P范围	解释率范围	染色体	SNP数量	-lg P范围	贡献率范围
1	26	2.068 54~4.190 81	0.052 81~0.110 93	14	19	2.002 61~3.925 59	0.051 64~0.105 60
2	14	2.037 63~2.600 33	0.053 75~0.071 00	15	19	2.018 18~3.392 17	0.053 42~0.097 52
3	20	2.080 40~8.906 37	0.053 88~0.227 68	16	20	2.002 18~3.256 40	0.051 70~0.086 90
4	10	1.274 66~4.011 90	0.053 13~0.086 69	17	13	2.062 98~3.935 54	0.056 49~0.085 32
5	20	2.021 82~3.791 88	0.052 90~0.101 19	18	10	2.028 26~2.557 52	0.052 32~0.068 71
6	15	2.048 66~3.624 94	0.054 89~0.100 13	19	28	2.040 01~3.675 18	0.038 05~0.098 28
7	33	2.017 73~3.899 15	0.058 34~0.107 22	20	16	2.003 93~3.493 91	0.051 71~0.094 90
8	24	2.003 05~3.902 85	0.052 64~0.101 25	21	16	2.068 54~5.305 96	0.055 92~0.146 60
9	8	2.011 89~2.920 82	0.053 10~0.076 02	22	14	2.032 92~3.729 37	0.052 75~0.104 19
10	22	2.060 48~3.485 21	0.053 71~0.094 63	23	17	2.005 24~3.549 60	0.053 08~0.077 53
11	31	2.014 12~3.316 12	0.051 87~0.089 56	24	23	2.034 33~9.322 39	0.052 48~0.265 20
12	28	2.026 87~3.287 20	0.055 55~0.088 94	25	12	2.364 52~3.221 60	0.061 59~0.068 63
13	13	2.004 36~2.463 44	0.037 09~0.066 66

染色体	SNP数量	-lg P范围	解释率范围	染色体	SNP数量	-lg P范围	贡献率范围
1	26	2.068 54~4.190 81	0.052 81~0.110 93	14	19	2.002 61~3.925 59	0.051 64~0.105 60
2	14	2.037 63~2.600 33	0.053 75~0.071 00	15	19	2.018 18~3.392 17	0.053 42~0.097 52
3	20	2.080 40~8.906 37	0.053 88~0.227 68	16	20	2.002 18~3.256 40	0.051 70~0.086 90
4	10	1.274 66~4.011 90	0.053 13~0.086 69	17	13	2.062 98~3.935 54	0.056 49~0.085 32
5	20	2.021 82~3.791 88	0.052 90~0.101 19	18	10	2.028 26~2.557 52	0.052 32~0.068 71
6	15	2.048 66~3.624 94	0.054 89~0.100 13	19	28	2.040 01~3.675 18	0.038 05~0.098 28
7	33	2.017 73~3.899 15	0.058 34~0.107 22	20	16	2.003 93~3.493 91	0.051 71~0.094 90
8	24	2.003 05~3.902 85	0.052 64~0.101 25	21	16	2.068 54~5.305 96	0.055 92~0.146 60
9	8	2.011 89~2.920 82	0.053 10~0.076 02	22	14	2.032 92~3.729 37	0.052 75~0.104 19
10	22	2.060 48~3.485 21	0.053 71~0.094 63	23	17	2.005 24~3.549 60	0.053 08~0.077 53
11	31	2.014 12~3.316 12	0.051 87~0.089 56	24	23	2.034 33~9.322 39	0.052 48~0.265 20
12	28	2.026 87~3.287 20	0.055 55~0.088 94	25	12	2.364 52~3.221 60	0.061 59~0.068 63
13	13	2.004 36~2.463 44	0.037 09~0.066 66

位点	基因型	基因型频率		χ²	等位基因	等位基因频率		χ²	P
位点	基因型	参考组	耐高温组	χ²	等位基因	参考组	耐高温组	χ²	P
rsc.646T>C	TT	33/0.465	22/0.733	6.705	T	98/0.690	50/0.833	4.415	0.035 6
	CC	6/0.085	2/0.067		C	44/0.310	10/0.167
	CT	32/0.451	6/0.200
rsc.777G>A	GG	33/0.465	22/0.733	6.705	G	98/0.690	50/0.833	4.415	0.035 6
	AA	6/0.085	2/0.067		A	44/0.310	10/0.167
	GA	32/0.451	6/0.200
rsc.966C>T	TT	5/0.070	2/0.067	5.237	C	99/0.697	49/0.817	3.074	0.079 5
	CC	33/0.465	21/0.700		T	43/0.303	11/0.183
	TC	33/0.465	7/0.233

联合GWAS和转录组分析挖掘与白斑狗鱼耐高温性状关联的SNP

Integrating GWAS and Transcriptome Profiling to Identify SNP Markers Linked to High-temperature Tolerance in Esox lucius

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