陆地棉吐絮率的限制性两阶段多位点全基因组关联分析及候选基因预测

doi:10.3864/j.issn.0578-1752.2022.02.002

中国农业科学 ›› 2022, Vol. 55 ›› Issue (2): 248-264.doi: 10.3864/j.issn.0578-1752.2022.02.002

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

陆地棉吐絮率的限制性两阶段多位点全基因组关联分析及候选基因预测

谢晓宇¹(),王凯鸿¹,秦晓晓¹,王彩香¹(),史春辉¹,宁新柱²,杨永林³,秦江鸿³,李朝周¹,马麒²(),宿俊吉¹()

¹甘肃农业大学生命科学技术学院/省部共建干旱生境作物学国家重点实验室,兰州 730070
²新疆农垦科学院棉花研究所,新疆石河子 832000
³石河子农业科学研究院,新疆石河子 832000

收稿日期:2021-08-13 接受日期:2021-10-26 出版日期:2022-01-16 发布日期:2022-01-26
通讯作者: 王彩香,马麒,宿俊吉
作者简介:谢晓宇,E-mail: xiexiaoyu0924@126.com。
基金资助:
国家自然科学基金(31971986);棉花生物学国家重点实验室开放课题(CB2021A03);棉花生物学国家重点实验室开放课题(CB2021A19);甘肃省科技计划(20JR10RA520);新疆兵团财政科技计划(2020DA001);甘肃农业大学国家级大学生创新创业训练计划(202110733018)

Restricted Two-Stage Multi-Locus Genome-Wide Association Analysis and Candidate Gene Prediction of Boll Opening Rate in Upland Cotton

XIE XiaoYu¹(),WANG KaiHong¹,QIN XiaoXiao¹,WANG CaiXiang¹(),SHI ChunHui¹,NING XinZhu²,YANG YongLin³,QIN JiangHong³,LI ChaoZhou¹,MA Qi²(),SU JunJi¹()

¹College of Life Science and Technology, Gansu Agricultural University/State Key Laboratory of Arid Land Crop Science, Lanzhou 730070
²Cotton Research Institute, Xinjiang Academy of Agricultural and Reclamation Science, Shihezi 832000, Xinjiang
³Shihezi Academy of Agriculture Science, Shihezi 832000, Xinjiang

Received:2021-08-13 Accepted:2021-10-26 Online:2022-01-16 Published:2022-01-26
Contact: CaiXiang WANG,Qi MA,JunJi SU

1. 电子附表.rar(69KB)

摘要/Abstract

摘要：

【目的】吐絮率是反映陆地棉（Gossypium hirsutum L.）早熟性状的重要指标之一,利用全基因组关联分析（genome-wide association study,GWAS）解析吐絮率的QTL（quantitative trait locus）及其遗传效应,为陆地棉早熟性状的分子育种提供理论基础。【方法】利用315份不同陆地棉品种（系）构成的自然群体,在3个环境下对吐絮率进行表型鉴定。同时利用前期构建的9 244个具有复等位变异SNP连锁不平衡区段（SNP linkage disequilibrium block,SNPLDB）分子标记,采用限制性两阶段多位点全基因组关联分析（restricted two-stage multi-locus GWAS,RTM-GWAS）方法,检测与吐絮率显著关联的SNPLDB位点、估算其表型效应值,并建立显著关联位点在群体中QTL-allele矩阵,鉴定稳定关联的主效SNPLDB位点及其优异单倍型。根据2组转录组数据的基因表达量,在显著SNPLDB位点侧翼序列1 Mb基因组范围内挖掘可能与目标性状有关的候选基因。【结果】陆地棉自然群体在3个环境下的吐絮率变异范围为37.78%—100.00%,广义遗传力为67.03%。多环境方差分析表明,吐絮率在基因型、环境及基因型×环境互作间均呈现极显著差异（P<0.001）。通过RTM-GWAS共检测到52个与吐絮率显著关联的SNPLDB位点,共包含179个等位基因/单倍型。其中90个增效等位基因/单倍型的效应值分布范围为0.014—19.43,89个减效等位基因/单倍型的效应值分布范围为-21.49—-0.039。在上述显著关联SNPLDB位点中,6个位点在多环境联合分析和单环境分析中均被检测到,被认为可能是与吐絮率显著关联的稳定SNPLDB位点。通过对上述6个稳定SNPLDB位点不同等位变异对应表型性状的差异显著性分析,鉴定出4个优异等位变异类型,分别为LDB_16_37952328（TT）、LDB_5_96395565（AA）、LDB_16_49503485（TT）和LDB_4_81118668（TT）。进一步分析发现,其优异等位变异的频率分布在中国4个不同生态区的品种（系）间存在差异。此外,在4个稳定主效SNPLDB位点的邻近区域共注释了178个基因,并利用转录组数据分析,预测发现其中23个基因可能是调控陆地棉吐絮率的候选基因。【结论】共鉴定到52个与吐絮率显著相关的SNPLDB位点,其中,有4个SNPLDB为稳定关联的主效位点;预测发现23个基因可能与陆地棉吐絮率有关。

关键词: 陆地棉, 吐絮率, 限制性两阶段多位点全基因组关联分析, QTL-等位基因矩阵, 候选基因

Abstract:

【Objective】Boll opening rate (BOR) is one of the most important indicators reflecting the early maturing trait of upland cotton (Gossypium hirsutum L.). The genome-wide association study (GWAS) was applied to dissect the QTL (quantitative trait locus) and its genetic effect for providing a theoretical basis for molecular breeding of early maturing traits in upland cotton. 【Method】The natural population composed of 315 different upland cotton varieties (lines) were used to identify the BOR under three environments. Simultaneously, a total of 9 244 SNP linkage disequilibrium block (SNPLDB) markers with multiple alleles were constructed. Then, the restricted two-stage multi-locus GWAS (RTM-GWAS) was utilized to detect SNPLDB loci significantly associated with BOR, estimate its phenotypic effect value, establish QTL-Allele matrix for significantly associated loci in the population, and further detected the stable major SNPLDB loci and elite haplotypes. Finally, according to the gene expression levels of the two transcriptome data, candidate genes that may be related to the target trait were mined within the 1 Mb genome range of the flanking sequence of the significant SNPLDB loci. 【Result】The variation of BOR was ranged from 37.78% to 100.00% and the broad-sense heritability was 67.03% in the natural population under three environments. The multi-environment variance analysis revealed that the BOR was significantly different among genotype, environment and genotype × environment interaction (P<0.001). A total of 52 SNPLDB loci significantly associated with BOR were detected through the RTM-GWAS procedure, containing 179 alleles or haplotypes, among them, the effect values of 90 increasing alleles or haplotypes ranged from 0.014 to 19.43, and the effect values of 89 decreasing alleles or haplotypes ranged from -21.49 to -0.039. Among the significant SNPLDB loci mentioned above, 6 SNPLDB loci were detected simultaneously in both multi-environment and single environment, which were considered as stable SNPLDB loci significantly associated with BOR. Through the significance analysis of phenotypic traits corresponding to different allelic variations of the above six stable SNPLDB loci, the four favorable alleles were identified as LDB_16_37952328(TT), LDB_5_96395565(AA), LDB_16_49503485(TT), and LDB_4_81118668(TT). Besides, further analysis showed that there were significant differences in the frequency distribution of favorable alleles among varieties (lines) in four different ecological regions. Additionally, a total of 178 genes were annotated and 23 potential candidate genes were predicted in the adjacent regions of 4 stable major SNPLDB loci by transcriptome data analysis. 【Conclusion】A total of 52 SNPLDB loci significantly associated with BOR were identified, of which 4 loci were stable major SNPLDB loci. Furthermore, it was predicted that 23 genes might be related to the BOR of upland cotton. These SNPLDBs loci and candidate genes will provide a theoretical basis for marker-assisted breeding of early maturity in upland cotton.

Key words: Upland cotton, boll opening rate, RTM-GWAS, QTL allele matrix, candidate genes

谢晓宇, 王凯鸿, 秦晓晓, 王彩香, 史春辉, 宁新柱, 杨永林, 秦江鸿, 李朝周, 马麒, 宿俊吉. 陆地棉吐絮率的限制性两阶段多位点全基因组关联分析及候选基因预测[J]. 中国农业科学, 2022, 55(2): 248-264.

XIE XiaoYu, WANG KaiHong, QIN XiaoXiao, WANG CaiXiang, SHI ChunHui, NING XinZhu, YANG YongLin, QIN JiangHong, LI ChaoZhou, MA Qi, SU JunJi. Restricted Two-Stage Multi-Locus Genome-Wide Association Analysis and Candidate Gene Prediction of Boll Opening Rate in Upland Cotton[J]. Scientia Agricultura Sinica, 2022, 55(2): 248-264.

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链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2022.02.002

https://www.chinaagrisci.com/CN/Y2022/V55/I2/248

图/表 8

表1

表2

表3

与陆地棉吐絮率显著关联的SNPLDB位点"

位点 Loci	染色体 Chr.	位置 Position (bp)	-lg(P)	表型变异 PV (%)	共同环境^a Common environments
LDB_16_37952328	16 (D03)	37952328	46.14	1.90	AY-15 (11.49)、SHZ-14 (5.91)
LDB_5_96395565	5 (A05)	96395565	22.69	0.40	AY-15 (7.42)
LDB_16_49503485	16 (D03)	49503485	17.79	0.91	AY-15 (8.49)
LDB_10_6908012	10 (A10)	6908012	16.70	0.87	AY-15 (8.75)
LDB_15_9697358	15 (D02)	9697358	13.52	1.89	AY-15 (8.41)
LDB_21_22036171	21 (D08)	22036171	13.44	1.34
LDB_4_81118668	4 (A04)	81118668	11.80	0.91	AY-15 (4.58)
LDB_3_6725154_6746183	3 (A03)	6725154	11.63	1.21
LDB_1_57527637_57527855	1 (A01)	57527637	10.44	1.11
LDB_16_36553916_36554161	16 (D03)	36553916	9.81	1.72
LDB_11_119047116	11 (A11)	119047116	9.76	0.86
LDB_19_52309050_52309284	19 (D06)	52309050	7.97	1.54
LDB_17_51465593	17 (D04)	51465593	7.93	0.51
LDB_13_54999733	13 (A13)	54999733	7.36	0.61
位点 Loci	染色体 Chr.	位置 Position (bp)	-lg(P)	表型变异 PV (%)	共同环境^a Common environments
LDB_20_6608424	20 (D07)	6608424	6.63
LDB_7_94884564_94884800	7 (A07)	94884564	6.34
LDB_19_53788858	19 (D06)	53788858	6.25	0.27
LDB_9_58666084_58666088	9 (A09)	58666084	6.06	1.12
LDB_6_41226103	6 (A06)	41226103	5.52	9.00
LDB_15_46384945_46385146	15 (D02)	46384945	5.17	0.36
LDB_15_67139952_67140180	15 (D02)	67139952	5.14	1.68
LDB_25_27281705	25 (D12)	27281705	5.10
LDB_23_6012092	23 (D10)	6012092	4.94	0.18
LDB_1_33221331	1 (A01)	33221331	4.06	0.38
LDB_12_96771402	12 (A12)	96771402	3.84	0.97
LDB_15_65780303	15 (D02)	65780303	3.65	0.67
LDB_22_48423583	22 (D09)	48423583	3.64	0.88
LDB_14_45778715_45778973	14 (D01)	45778715	3.58	1.08
LDB_21_5030313_5030325	21 (D08)	5030313	3.55	0.15
LDB_25_39776065	25 (D12)	39776065	3.47	0.37
LDB_26_45642548	26 (D13)	45642548	3.42		SHZ-14 (1.77)
LDB_5_30493466	5 (A05)	30493466	3.20
LDB_12_103902963	12 (A12)	103902963	3.15	0.39
LDB_3_42046528_42046540	3 (A03)	42046528	2.86
LDB_10_70110862_70110882	10 (A10)	70110862	2.51
LDB_13_72681594_72681843	13 (A13)	72681594	2.46	0.21
LDB_19_39327466	19 (D06)	39327466	2.43
LDB_11_18062977	11 (A11)	18062977	2.42	0.44
LDB_8_113962673	8 (A08)	113962673	2.30
LDB_23_24053424	23 (D10)	24053424	2.25	0.43
LDB_21_25090078	21 (D08)	25090078	2.19	0.47
LDB_6_108270563	6 (A06)	108270563	2.05
LDB_25_1835041	25 (D12)	1835041	1.86	0.18
LDB_2_4064617	2 (A02)	4064617	1.76	0.29
LDB_18_52473670	18 (D05)	52473670	1.71	0.32
LDB_13_62696637	13 (A13)	62696637	1.62	0.30
LDB_8_8677270	8 (A08)	8677270	1.56
LDB_24_59986795	24 (D11)	59986795	1.48
LDB_17_1478345	17 (D04)	1478345	1.39	0.42
LDB_5_23314512	5 (A05)	23314512	1.34
LDB_15_17739938	15 (D02)	17739938	1.34
LDB_17_53762505_53762526	17 (D04)	53762505	1.33		AY-14 (4.68)

表3

图1

图2

图3

图4

表4

与陆地棉吐絮率相关的候选基因"

组别 Group	候选基因 Candidate gene	基因名称 Gene name	基因功能注释 Gene function annotation
a类 Group a	GH_D03G1078	SWEET10	双向糖转运体SWEET10 Bidirectional sugar transporter SWEET10
	GH_D03G1058	slc25a24	钙结合线粒体载体蛋白 SCAMC-1 Calcium-binding mitochondrial carrier protein SCaMC-1
	GH_D03G1629	IRL5	植物细胞内Ras-group相关LRR蛋白5 Plant intracellular Ras-group-related LRR protein 5
	GH_D03G1059	NA	NA
	GH_D03G1067	Bicc1	蛋白双尾C同源物1 Protein bicaudal C homolog 1
	GH_D03G1594	RABD2C	Ras-related蛋白质RABD2c Ras-related protein RABD2c
	GH_D03G1618	NA	假定的转化酶抑制剂 Putative invertase inhibitor
	GH_A04G1255	RRP6L3	蛋白质RRP6-like 3 Protein RRP6-like 3
	GH_D03G1643	ABCB2	ABC转运体B家族成员2 ABC transporter B family member 2
b类 Group b	GH_D03G1586	HOS1	E3泛素蛋白连接酶HOS1 E3 ubiquitin-protein ligase HOS1
	GH_D03G1616	BRG3	可能与BOI相关的E3泛素蛋白连接酶3 Probable BOI-related E3 ubiquitin-protein ligase 3
	GH_A04G1248	P3H1	脯氨酰3-羟化酶 1 Prolyl 3-hydroxylase 1
	GH_D03G1644	HSF8	热休克因子蛋白HSF8 Heat shock factor protein HSF8
c类 Group c	GH_D03G1617	UPF1	无意义转录本1同源物的调节器 Regulator of nonsense transcripts 1 homolog
	GH_D03G1083	NA	NA
	GH_D03G1610	caskin2	Caskin-2
	GH_A04G1266	SPL6	Squamosa启动子结合样蛋白6 Squamosa promoter-binding-like protein 6
	GH_D03G1087	PAP27	可能失活的紫色酸性磷酸酶27 Probable inactive purple acid phosphatase 27
	GH_D03G1608	At2g01680	含锚蛋白重复蛋白At2g01680 Ankyrin repeat-containing protein At2g01680
	GH_D03G1063	GLO1	过氧化物酶体(S)-2-羟基氧化酶 Peroxisomal (S)-2-hydroxy-acid oxidase GLO1
	GH_D03G1085	IRX15	蛋白质不规则木质部15 Protein IRREGULAR XYLEM 15
	GH_A05G3660	At3g52300	ATP合酶亚基d,线粒体 ATP synthase subunit d, mitochondrial
	GH_A05G3680	NA	NA

表4

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性状 Trait	方差来源 Variance	平方和 SS	均方 MS	F值 F- value	P值 P-value	遗传力 H²(%)
吐絮率 BOR	环境Environment	321981.19	160990.59	1084.69	<0.0001	67.03
	基因型Genotype	288095.59	917.50	6.18	<0.0001
	环境×基因型Environment ×Genotype	237515.09	378.21	2.55	<0.0001

陆地棉吐絮率的限制性两阶段多位点全基因组关联分析及候选基因预测

Restricted Two-Stage Multi-Locus Genome-Wide Association Analysis and Candidate Gene Prediction of Boll Opening Rate in Upland Cotton

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环境 Env.	吐絮率BOR(%)																平均数 Mean (%)	变幅 Range (%)	变异系数 CV (%)
环境 Env.	13	19	25	31	37	43	49	55	61	67	73	79	85	91	97	N	平均数 Mean (%)	变幅 Range (%)	变异系数 CV (%)
AY-14							3	5	6	19	31	85	133	33		315	80.62	46.73—90.00	9.86
AY-15	4	5	11	23	25	32	35	43	36	22	24	20	19	9	7	315	55.99	10.42—100.00	34.60
SHZ-14					1	1	3	16	28	41	63	62	57	34	9	315	70.80	37.78—98.05	14.42
综合 Syn.					1	2	9	24	48	58	80	44	37	12		315	70.76	39.27—91.32	14.25

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