东北大豆种质群体百粒重QTL-等位变异的全基因组解析

doi:10.3864/j.issn.0578-1752.2020.09.003

中国农业科学 ›› 2020, Vol. 53 ›› Issue (9): 1717-1729.doi: 10.3864/j.issn.0578-1752.2020.09.003

所属专题：专题——限制性两阶段多位点全基因组关联分析法的应用

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东北大豆种质群体百粒重QTL-等位变异的全基因组解析

郝晓帅¹,傅蒙蒙¹,刘再东¹,贺建波¹(),王燕平²,任海祥²,王德亮³,杨兴勇⁴,程延喜⁵,杜维广²,盖钧镒¹()

¹ 南京农业大学大豆研究所/国家大豆改良中心/农业部大豆生物学与遗传育种重点实验室/作物遗传与种质创新国家重点实验室/江苏省现代作物生产协同创新中心,南京 210095;
² 黑龙江省农业科学院牡丹江分院/国家大豆改良中心牡丹江试验站,黑龙江牡丹江 157041;
³ 黑龙江省农垦科学院,黑龙江佳木斯 154007;
⁴ 黑龙江省农业科学院克山分院,黑龙江克山 161606;
⁵ 长春市农业科学院,长春 130111

收稿日期:2019-09-09 接受日期:2020-01-02 出版日期:2020-05-01 发布日期:2020-05-13
联系方式: 郝晓帅,E-mail：15850563928@163.com。
基金资助:
国家自然科学基金(31701447);国家作物育种重点研发计划(2017YFD0101500);国家作物育种重点研发计划(2017YFD0102002);长江学者和创新团队发展计划(PCSIRT_17R55);教育部111项目(B08025);中央高校基本科研业务费项目(KYT201801);农业部国家大豆产业技术体系CARS-04;江苏省优势学科建设工程专项;江苏省JCIC-MCP项目

Genome-Wide QTL-Allele Dissection of 100-Seed Weight in the Northeast China Soybean Germplasm Population

XiaoShuai HAO¹,MengMeng FU¹,ZaiDong LIU¹,JianBo HE¹(),YanPing WANG²,HaiXiang REN²,DeLiang WANG³,XingYong YANG⁴,YanXi CHENG⁵,WeiGuang DU²,JunYi GAI¹()

¹ Soybean Research Institute, Nanjing Agricultural University/National Center for Soybean Improvement/Key Laboratory of Biology and Genetic Improvement of Soybean (General), Ministry of Agriculture/State Key Laboratory for Crop Genetics and Germplasm Enhancement/Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing 210095;
² Mudanjiang Branch of Heilongjiang Academy of Agricultural Sciences/Mudanjiang Experiment Station of the National Center for Soybean Improvement, Mudanjiang 157041, Heilongjiang;
³ Heilongjiang Academy of Land-reclamation Sciences, Jiamusi 154007, Heilongjiang;
⁴ Keshan Branch of Heilongjiang Academy of Agricultural Sciences, Keshan 161606, Heilongjiang;
⁵ Changchun Academy of Agricultural Sciences, Changchun 130111

Received:2019-09-09 Accepted:2020-01-02 Published:2020-05-01 Online:2020-05-13

摘要/Abstract

摘要：

【目的】对东北大豆种质群体百粒重性状进行全基因组关联分析,全面解析中国大豆主产区百粒重QTL-等位变异遗传构成,为东北地区大豆籽粒大小遗传改良提供理论基础。【方法】以东北地区育种和生产上常用的290份大豆材料作为试验群体,于2013和2014年在东北第二生态亚区的克山、牡丹江、佳木斯和长春4个地点进行百粒重表型鉴定试验。利用RAD-seq方法对试验群体进行基因组测序分析,对原始SNP数据进行过滤及填补缺失数据后,最终获得了82 966个高质量的SNP标记。根据限制性两阶段多位点全基因组关联分析（restricted two-stage multi-locus genome-wide association analysis,RTM-GWAS）方法,首先构建获得15 546个具有复等位变异的SNPLDB标记,然后使用两阶段多位点模型对百粒重性状进行全基因组关联分析。对检测到的百粒重关联SNPLDB标记位点附近（50 kb范围内）的基因进行分析,根据基因内SNP与SNPLDB标记位点之间关联性的卡方测验,筛选可能与百粒重性状相关的候选基因并进行功能注释。最后基于检测的百粒重QTL-等位变异体系分析了不同熟期组材料间的遗传分化。【结果】试验群体百粒重变异范围为18.3—20.7 g,性状遗传率为92.3%。RTM-GWAS方法共检测到76个与大豆百粒重性状关联的SNPLDB标记位点,其中15个位点主效不显著,另外61个主效显著位点解释了65.40%的表型变异;68个与环境互作效应显著的位点解释了17.46%的表型变异,另外8个位点与环境互作效应不显著。在检测到的76个位点中有34个位点与已报道的30个百粒重QTL重叠,另外42个位点为本研究新检测百粒重位点。基于检测的SNPLDB标记位点,共筛选到137个百粒重相关候选基因,功能注释显示这些候选基因不仅参与大豆百粒重的调节,还参与了初级新陈代谢、蛋白质修饰、物质运输、胁迫响应和信号转导等。对各熟期组间QTL-等位变异的遗传分化分析显示,尽管熟期组间百粒重差异不明显,但其QTL-等位变异遗传结构却发生了新生和汰除的变化。【结论】RTM-GWAS方法能相对全面地解析东北大豆种质群体百粒重QTL-等位变异遗传构成。东北大豆种质群体百粒重由大量QTL调控,且QTL与环境互作效应大,QTL存在丰富的复等位变异。由RTM-GWAS方法建立的QTL-等位变异矩阵为群体遗传及演化研究提供了新工具。

关键词: 大豆, 百粒重, 限制性两阶段多位点全基因组关联分析, QTL-allele矩阵, 候选基因

Abstract:

【Objective】A genome-wide association study in the Northeast China soybean germplasm population was conducted for a relatively thorough detection of the QTL-allele constitution of 100-seed weight, which may provide a theoretical basis for soybean breeding for seed size improvement. 【Method】In the present study, a total of 290 soybean accessions that were frequently used for soybean breeding and production in the Northeast China were tested in 2013 and 2014 for 100-seed weight at four locations, including Keshan, Mudanjiang, Jiamusi and Changchun, which are all in the second sub-ecoregion of the Northeast China. RAD-seq (restriction site-associated DNA sequencing) was used for SNP genotyping, and 82 966 high-quality SNPs were obtained after filtering and imputation. According to the RTM-GWAS (restricted two-stage multi-locus genome-wide association analysis) method, firstly a total of 15 546 multi-allelic SNPLDBs were constructed, and then a multi-locus model was used for genome-wide association study of 100-seed weight. The genes near (within 50kb) the detected SNPLDBs were analyzed, and candidate genes for 100-seed weight were identified and annotated according to Chi-square test of independence between the SNPs within genes and the detected SNPLDBs. Finally, genetic differentiation among maturity groups were investigated based on the detected QTL-allele system of 100-seed weight. 【Result】The 100-seed weight of the present population ranged from 18.3 to 20.7 g, and the trait heritability was 92.3%. A total of 76 SNPLDBs were detected to be associated with 100-seed weight, among which there were 15 SNPLDBs with non-significant main effect and the 61 SNPLDBs with significant main effect explained 65.40% phenotypic variation. There were 68 SNPLDBs that had significant interaction effect with environment and explained 17.46% phenotypic variation. In addition, 34 out of 76 detected SNPLDBs overlapped 30 previously reported QTLs and 42 SNPLDBs were novel loci. A total of 137 candidate genes for 100-seed weight were annotated in the detected SNPLDB regions, and functional annotation showed that these genes were not only involved in regulation of 100-seed weight, but also involved in primary metabolism, translation, protein modification, material transport, stress response and signal transduction, etc. Although there was no obvious difference in the 100-seed weight among different maturity groups, genetic differentiation analysis showed varying changes of allele emergence and exclusion in QTL-allele structure of 100-seed weight among maturity groups. 【Conclusion】The RTM-GWAS method used in the present study provided a relatively thorough detection of genome-wide QTLs and their multiple alleles for 100-seed weight in the Northeast China soybean germplasm population. The 100-seed weight of the Northeast China soybean germplasm population was controlled by a large number of QTLs with large significant interaction effect with environment, and there was also abundant multiple allelic variation in these QTLs. The QTL-allele matrix established from RTM-GWAS provided an efficient tool for population genetics and evolution study.

Key words: soybean [Glycine max (L.) Merr.], 100-seed weight, RTM-GWAS, QTL-allele matrix, candidate gene

郝晓帅,傅蒙蒙,刘再东,贺建波,王燕平,任海祥,王德亮,杨兴勇,程延喜,杜维广,盖钧镒. 东北大豆种质群体百粒重QTL-等位变异的全基因组解析[J]. 中国农业科学, 2020, 53(9): 1717-1729.

XiaoShuai HAO,MengMeng FU,ZaiDong LIU,JianBo HE,YanPing WANG,HaiXiang REN,DeLiang WANG,XingYong YANG,YanXi CHENG,WeiGuang DU,JunYi GAI. Genome-Wide QTL-Allele Dissection of 100-Seed Weight in the Northeast China Soybean Germplasm Population[J]. Scientia Agricultura Sinica, 2020, 53(9): 1717-1729.

图/表 6

表1

表2

图1

表3

大豆百粒重显著相关SNPLDB位点"

QTL	AN	主效QTL		QTL×Env. ^a		QTL	AN	主效QTL		QTL×Env. ^a
QTL	AN	-lgP	R² (%)	-lgP	R² (%)	QTL	AN	-lgP	R² (%)	-lgP	R² (%)
q-SW-1-1	2	-	-	6.07	0.10	q-SW-12-1	2	7.95	0.08	6.99	0.11
q-SW-1-2	2	-	-	3.47	0.06	q-SW-12-2	8	4.34	0.07	4.63	0.24
q-SW-1-3	2	-	-	2.55	0.05	q-SW-12-3	4	5.30	0.06	20.46	0.35
q-SW-2-1	5	2.87	0.04	7.60	0.21	q-SW-12-4	2	2.27	0.02	3.83	0.07
q-SW-2-2	3	-	-	2.85	0.06	q-SW-12-5	2	-	-	3.50	0.06
q-SW-2-3	5	203.54	2.40	11.07	0.26	q-SW-13-1	6	150.15	1.76	20.04	0.42
q-SW-2-4	2	-	-	2.29	0.05	q-SW-13-2	7	76.04	0.90	46.13	0.80
q-SW-2-5	2	13.60	0.14	-	-	q-SW-13-3	5	28.30	0.33	14.53	0.31
q-SW-2-6	2	3.00	0.03	-	-	q-SW-13-4	4	102.12	1.16	10.74	0.23
q-SW-3-1	3	5.73	0.06	-	-	q-SW-14-1	7	-	-	7.12	0.26
q-SW-3-2	6	3.19	0.05	12.21	0.31	q-SW-14-2	6	192.85	2.28	19.05	0.41
q-SW-3-3	5	307.65	4.26	18.50	0.37	q-SW-14-3	2	63.12	0.69	-	-
q-SW-3-4	4	-	-	4.81	0.14	q-SW-14-4	2	-	-	2.26	0.05
q-SW-4-1	6	19.08	0.24	5.81	0.21	q-SW-15-1	6	34.07	0.41	7.51	0.24
q-SW-4-2	5	14.91	0.18	10.54	0.26	q-SW-15-2	6	40.33	0.48	15.05	0.35
q-SW-4-3	2	307.65	10.56	-	-	q-SW-16-1	3	213.17	2.49	3.98	0.10
q-SW-4-4	6	59.53	0.70	12.31	0.31	q-SW-16-2	4	-	-	11.03	0.23
q-SW-6-1	2	35.63	0.38	3.29	0.06	q-SW-16-3	2	2.74	0.02	2.41	0.05
q-SW-6-2	6	8.46	0.11	8.63	0.26	q-SW-16-4	5	20.46	0.24	14.44	0.31
q-SW-6-3	2	2.61	0.02	2.41	0.05	q-SW-16-5	7	29.99	0.37	19.95	0.45
q-SW-6-4	7	29.03	0.36	23.57	0.50	q-SW-17-1	5	53.76	0.62	7.77	0.21
q-SW-6-5	8	7.57	0.12	6.58	0.27	q-SW-17-2	5	2.98	0.04	26.98	0.48
q-SW-6-6	3	35.92	0.40	3.54	0.09	q-SW-18-1	5	145.14	1.69	4.18	0.16
q-SW-6-7	4	49.75	0.56	8.91	0.20	q-SW-18-2	2	-	-	2.29	0.05
q-SW-7-1	5	12.92	0.16	15.52	0.33	q-SW-18-3	6	262.05	3.16	31.38	0.57
q-SW-7-2	2	147.28	1.66	2.36	0.05	q-SW-18-4	7	17.23	0.22	13.01	0.35
q-SW-7-3	6	11.66	0.15	10.25	0.28	q-SW-18-5	2	-	-	5.50	0.09
q-SW-8-1	2	-	-	4.40	0.08	q-SW-18-6	4	200.62	2.35	10.23	0.22
q-SW-8-2	3	90.82	1.02	4.07	0.10	q-SW-18-7	5	228.35	2.71	88.81	1.24
q-SW-8-3	2	-	-	-	-	q-SW-19-1	8	15.85	0.21	10.59	0.32
q-SW-8-4	2	45.35	0.49	-	-	q-SW-19-2	7	178.86	2.12	14.09	0.37
q-SW-8-5	4	114.44	1.31	8.39	0.19	q-SW-19-3	7	54.88	0.64	16.95	0.38
q-SW-9-1	2	-	-	2.12	0.05	q-SW-19-4	6	74.96	0.87	11.80	0.30
q-SW-9-2	6	8.40	0.11	10.50	0.28	q-SW-19-5	5	23.13	0.27	5.86	0.18
q-SW-9-3	2	24.99	0.26	4.68	0.08	q-SW-20-1	8	307.65	5.77	55.70	0.97
q-SW-9-4	6	59.00	0.69	17.45	0.39	q-SW-20-2	5	34.46	0.40	13.88	0.30
q-SW-9-5	6	95.80	1.11	14.16	0.34	LC-QTL	83	18	52.15
q-SW-10-1	5	6.28	0.08	3.34	0.14	SC-QTL	205	43	13.25
q-SW-10-2	2	307.65	4.35	7.36	0.11	总Total	328	61	65.40	68	17.46
q-SW-10-3	2	89.96	0.99	-	-

表3

表4

百粒重性状相关大效应QTL和候选基因"

QTL	R² (%)	候选基因 Candidate gene	基因本体生物学过程 Gene ontology biological process
q-SW-3-3	4.43	Glyma03g31790	囊泡介导的运输Vesicle-mediated transport
		Glyma03g31810	线粒体mRNA修饰Mitochondrial mRNA modification
		Glyma03g31820	微管细胞骨架组织Microtubule cytoskeleton organization
		Glyma03g31940	甲壳素响应Response to chitin
		Glyma03g32040	高尔基体内囊泡介导转运Intra-Golgi vesicle-mediated transport
q-SW-4-3	10.93	Glyma04g38830	细胞分裂素代谢Cytokinin metabolic
		Glyma04g38870	甲基转移酶活性Methyltransferase activity
		Glyma04g38955	糖介导的信号通路Sugar mediated signaling pathway
q-SW-8-5	1.36	Glyma08g44800	RRNA加工RRNA processing
		Glyma08g44820	蛋白水解Proteolysis
		Glyma08g44960	未知Unknown
		Glyma08g44921	跨膜运输Transmembrane transport
q-SW-9-5	1.16	Glyma09g41070	液泡运输Vacuolar transport
		Glyma09g41140	肌醇六磷酸磷酸酯的生物合成过程Myo-inositol hexakisphosphate biosynthetic process
		Glyma09g41150	胚胎发育以种子休眠结束Embryo development ending in seed dormancy
		Glyma09g41260	氧化应激响应Response to oxidative stress
		Glyma09g41320	鸟嘌呤运输Guanine transport
		Glyma09g41121	未知Unknown
q-SW-13-1	1.83	Glyma13g08170	翻译调控Regulation of translation
q-SW-13-4	1.21	Glyma13g29011	种子萌发Seed germination
q-SW-14-2	2.37	Glyma14g08040	嘧啶核糖核苷酸生物合成Pyrimidine ribonucleotide biosynthetic
		Glyma14g08050	缺氧响应Response to hypoxia
		Glyma14g08070	种子萌发正调控Positive regulation of seed germination
		Glyma14g08220	脱落酸应激响应Response to abscisic acid stimulus
		Glyma14g08075	未知Unknown
		Glyma14g08145	未知Unknown
q-SW-16-1	2.58	Glyma16g06320	未知Unknown
q-SW-18-1	1.75	Glyma18g10460	新陈代谢Metabolic
		Glyma18g10470	防御反应Defense response
q-SW-18-3	3.28	Glyma18g16720	蛋白质折叠Protein folding
		Glyma18g16761	蛋白水解Proteolysis
q-SW-18-6	2.44	Glyma18g36455	未知Unknown
q-SW-18-7	2.81	Glyma18g52250	盐胁迫响应Response to salt stress
		Glyma18g52260	转录调控Regulation of transcription
		Glyma18g52290	碳水化合物代谢Carbohydrate metabolic
		Glyma18g52350	Basipetal生长素运输Basipetal auxin transport

表4

表5

百粒重QTL-等位变异在熟期组间的变化"

QTL	a1	a2	a3	a4		a5	a6	a7	a8		QTL	a1	a2	a3	a4	a5	a6	a7	a8		QTL	a1	a2	a3	a4	a5	a6	a7	a8
1-1	yz										7-3			X	yz						14-4	yz
1-2		y									8-1		z								15-1				X
1-3		yz									8-2			z							15-2	z	z
2-1	z					z					8-3	XYZ	yz		XZ						16-1
2-2	z	yz									8-4	xyz	XYZ	XYZ	XYZ	XYZ	xyz				16-2			XY	yz
2-3	X			XY		z					8-5	xyz	xyz	xyz	xyz						16-3
2-4	XZ										9-1	z									16-4	yz
2-5		z									9-2	xy	z								16-5	yz	z
2-6	yz										9-3		XY								17-1		XY			z
3-1	XY		XYZ	Y							9-4				XYZ	y	z				17-2	z				y
3-2	X		XZ								9-5			yz							18-1	XYZ	y			z
3-3	yz		yz								10-1	X			XY						18-2		z
3-4		z		y							10-2		X								18-3	y		z		z	yz
4-1		yz	yz	yz		z					10-3		z								18-4				yz	yz	yz	XY
4-2	z	yz		yz							12-1										18-5	yz
4-3	z										12-2	z	XZ		yz		z	z	yz		18-6	yz	yz	y
4-4	YZ	yz	xz			z	z				12-3	yz	z								18-7				z
6-1											12-4		yz								19-1							X
6-2	z						X				12-5	z									19-2		z	xyz	z
6-3		XZ									13-1				z	yz	z				19-3			XY			XY
6-4			z	yz			z				13-2	z	yz		XZ	z					19-4	yz		yz		z	YZ
6-5		yz	y			yz		y	yz		13-3			z	XYZ	z					19-5					z
6-6	yz	yz									13-4			z	yz						20-1	XZ	X		z	y	yz	XY	X
6-7			xyz								14-1	yz		z		z					20-2	y				y
7-1	XYZ			z							14-2	XYZ	XY		yz
7-2											14-3		xy
熟期组 Maturity group					等位变异总数 Total allele					继承等位变异 Inherent allele						变化等位变异 Changed allele				新生等位变异 Emerged allele						汰除等位变异 Excluded allele
熟期组 Maturity group					Allele no.			QTL no.		Allele no.				QTL no.		Allele no.		QTL no.		Allele no.				QTL no.		Allele no.			QTL no.
Ⅰ+Ⅱ					292 (147, 145)			76
0 vs.Ⅰ+Ⅱ					321 (162, 159)			76		287 (144, 143)				76		39 (21,18)		30		34 (18,16)				25		5 (3,2)			5
00 vs. 0					250 (125,125)			76		247 (123, 124)				76		77(41,36)		49		3 (2,1)				2		74 (39,35)			49
000 vs. 00					208 (105,103)			76		189 (96,93)				76		80(38,42)		52		19 (9,10)				17		61(29,32)			44
0+00+000 vs.Ⅰ+Ⅱ					324 (163, 161)			76		288 (144, 144)				76		40 (22,18)		31		36 (19,17)				27		4(3,1)			4

表5

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模型Model	变异来源Source	自由度DF	均方MS	F	p
基因型×年份×地点 Genotype×Year×Location	年份Year	1	835.46	81.59	<0.001
	地点Location	3	3156.29	493.80	<0.001
	区组（年份,地点） Block(Year, Location)	24	2.59	1.86	0.0068
	基因型Genotype	289	146.47	13.74	<0.001
	基因型×年份Genotype×Year	289	9.10	2.65	<0.001
	基因型×地点Genotype×Location	867	5.22	1.41	<0.001
	基因型×年份×地点Genotype×Year×Location	849	3.70	2.65	<0.001
	误差Error	6791	1.40
基因型×环境 Genotype×Environment	环境Environment	7	1978.57	308.84	<0.001
	区组（环境） Block(Environment)	24	2.59	1.86	0.0068
	基因型Genotype	289	147.00	28.15	<0.001
	基因型×环境Genotype×Environment	2005	5.24	3.75	<0.001
	误差Error	6791	1.40

东北大豆种质群体百粒重QTL-等位变异的全基因组解析

Genome-Wide QTL-Allele Dissection of 100-Seed Weight in the Northeast China Soybean Germplasm Population

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类型 Type	百粒重100-seed weight (g)															N	平均数 Mean	变幅 Range	遗传率 h²
类型 Type	7	9	11	12	14	16	17	19	21	23	24	26	28	29	31	N	平均数 Mean	变幅 Range	遗传率 h²
环境Environment
长春CC		1	1	0	0	9	45	75	85	52	14	4	4			290	20.3	9.7-28.2	0.642
佳木斯JMS	1	2	10	3	1	1	17	57	93	68	28	4	4	0	1	290	20.7	8.1-32.0	0.780
克山KS	3	2	0	1	5	45	91	83	49	9	1	0	1			290	18.3	6.4-28.2	0.777
牡丹江MDJ		2	0	0	0	10	48	98	85	39	4	3	0	1		290	19.9	6.7-28.9	0.726
Mean		1	1	0	0	7	53	89	90	39	5	4	0	1		290	19.8	8.2-29.5	0.923
熟期组Maturity
MG0					1	2	25	55	51	16	4	1				155	19.9	13.6-25.6
MG00			1	0	0	0	6	11	15	10	2					45	20.3	9.9-24.8
MG000							3	3	5	3	1					15	20.4	18.8-21.8
MGI+II						2	9	33	25	6						75	19.7	15.6-22.7
MG0+00+000			1	0	1	2	34	69	71	29	7	1				215	20.0	9.9-25.6

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