玉米籽粒淀粉含量全基因组关联分析和候选基因预测

doi:10.3724/SP.J.1006.2023.23020

作物学报 ›› 2023, Vol. 49 ›› Issue (1): 140-152.doi: 10.3724/SP.J.1006.2023.23020

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

玉米籽粒淀粉含量全基因组关联分析和候选基因预测

王锐璞¹(), 董振营¹^,²(), 高悦欣¹, 鲍建喜¹, 殷芳冰¹, 李金萍², 龙艳¹^,²^,^*(), 万向元¹^,²^,^*()

¹北京科技大学生物与农业研究中心 / 化学与生物工程学院 / 顺德研究生院 / 北京中智生物农业国际研究院, 北京 100083
²北京首佳利华科技有限公司 / 主要作物生物育种北京市工程实验室 / 生物育种北京市国际科技合作基地, 北京 100192

收稿日期:2022-02-27 接受日期:2022-05-05 出版日期:2023-01-12 网络出版日期:2022-05-24
通讯作者: 龙艳,万向元
作者简介:王锐璞, E-mail: 15903575520@163.com;
董振营, E-mail: zydong@ustb.edu.cn第一联系人：^**同等贡献
基金资助:
国家重点研发计划项目“农业生物种质资源挖掘与创新利用”重点专项(2021YFD1200700)

Genome-wide association study and candidate gene prediction of kernel starch content in maize

WANG Rui-Pu¹(), DONG Zhen-Ying¹^,²(), GAO Yue-Xin¹, BAO Jian-Xi¹, YIN Fang-Bing¹, LI Jin-Ping², LONG Yan¹^,²^,^*(), WAN Xiang-Yuan¹^,²^,^*()

¹Zhongzhi International Institute of Agricultural Biosciences, Shunde Graduate School, School of Chemistry and Biological Engineering, Research Center of Biology and Agriculture, University of Science and Technology Beijing (USTB), Beijing 100083, China
²Beijing Engineering Laboratory of Main Crop Bio-Tech Breeding, Beijing International Science and Technology Cooperation Base of Bio-Tech Breeding, Beijing Solidwill Sci-Tech Co. Ltd., Beijing 100192, China

Received:2022-02-27 Accepted:2022-05-05 Published:2023-01-12 Published online:2022-05-24
Contact: LONG Yan,WAN Xiang-Yuan
About author:First author contact:^**Contributed equally to this work
Supported by:
National Key Research and Development Program of China(2021YFD1200700)

摘要/Abstract

摘要：

玉米是重要的粮食作物, 其籽粒重量的70%来自于淀粉。淀粉不仅是人类及其他动物的主要能量来源, 同时也是化工等行业的重要原料。本研究利用711份玉米自交系作为关联群体, 对2个环境下玉米籽粒湿基淀粉含量和干基淀粉含量进行统计分析, 结合覆盖玉米全基因组的2799个单核苷酸多态性(single nucleotide polymorphism, SNP)标记, 通过FarmCPU模型对玉米籽粒淀粉含量性状开展全基因组关联分析(genome-wide association study, GWAS), 共关联到67个显著SNP位点, 其中23个高可信度显著SNP位点可在多个环境重复检测到。3个高可信度SNP标记位点为本研究首次发现与玉米籽粒淀粉含量相关, 其余20个SNP标记位于前人已定位QTL (quantitative trait locus)置信区间或/和已报道与籽粒淀粉含量显著相关SNP标记1 Mb之内。进一步通过基因功能注释、基因本体论(gene ontology, GO)分析及籽粒胚乳基因表达分析, 在23个高可信度显著SNP位点上下游各200 kb候选区间共挖掘45个重要候选基因, 涉及淀粉生物合成与代谢、碳水化合物代谢、糖代谢、激素代谢等途径, 同时检测到2个已报道调控玉米籽粒淀粉含量的基因Ae1和Pin1。通过等位变异效应分析鉴定出9个主效SNP位点及其优异等位变异。本研究为深入解析玉米籽粒淀粉含量遗传机制提供了新的信息, 为加速培育高产、优质玉米新品种提供重要基因资源。

关键词: 玉米, 籽粒淀粉含量, 全基因组关联分析, 候选基因

Abstract:

Maize is an important food crop worldwide, and about 70% of its grain weight comes from starch. Starch is not only the main energy resource for human and other animals but also an important raw material for chemical industries. In this study, an association panel including 711 maize inbred lines was used for the examination of both wet-base starch content and dry-base starch content of maize kernel from two environments combined with 2799 single nucleotide polymorphism (SNP) markers spaning the whole genome of maize, genome-wide association study (GWAS) was carried out using FarmCPU model. 67 significant SNPs were identified, of which 23 highly reliable significant SNPs (HRS-SNPs) could be repeatedly associated in different environments. Three HRS-SNPs were reported for the first time by our study, and the remaining 20 HRS-SNPs were either located within the known quantitative trait loci (QTLs) or within 1 Mb of known SNPs associated with mazie kernel starch content. Through gene function annotation, gene ontology (GO) analysis and gene expression analysis, a total of 45 important candidate genes, involving starch biosynthesis, carbohydrate metabolism, sugar metabolism, hormone metabolism, and other pathways were identified within 200 kb regions around the HRS-SNPs. And two genes Ae1 and Pin1 which had been reported to regulate the maize kernel starch content were also detected. Furthermore, elite alles of the nine major SNPs was identified by allelic variation effect analysis. Our study provides new genetic information for further disecting the genetic mechanism of maize kernel starch content and provides important gene resources for accelerating the breeding of new maize varieties with high yield and quality.

Key words: maize, kernel starch content, genome-wide association study, candidate gene

王锐璞, 董振营, 高悦欣, 鲍建喜, 殷芳冰, 李金萍, 龙艳, 万向元. 玉米籽粒淀粉含量全基因组关联分析和候选基因预测[J]. 作物学报, 2023, 49(1): 140-152.

WANG Rui-Pu, DONG Zhen-Ying, GAO Yue-Xin, BAO Jian-Xi, YIN Fang-Bing, LI Jin-Ping, LONG Yan, WAN Xiang-Yuan. Genome-wide association study and candidate gene prediction of kernel starch content in maize[J]. Acta Agronomica Sinica, 2023, 49(1): 140-152.

图/表 9

表1

附图1

表2

附图2

图1

附表1

本研究所鉴定67个玉米籽粒淀粉含量关联分析显著SNP信息"

关联位点 Associated SNP	染色体 Chr.	位置 Position (bp)	P 值 P-value	表型变异率 PVE (%)	性状及环境 Trait and environment
SYN20034	1	13,864,423	4.83E-05	0.94	C^*
PZE-101026314	1	16,041,430	1.16E-04	1.22	A
PZE-101058274	1	42,284,401	8.48E-04	2.56	D
PZE-101060842	1	44,730,532	4.27E-05	2.89	E, F
PZE-101099263	1	93,135,341	2.46E-05	0.13	B
PZE-101105385	1	109,861,210	3.43E-04	0.76	D
PZE-101107894	1	115,245,510	4.01E-07	2.86	A, C, D, F
PZE-101117618	1	144,859,179	9.63E-04	0.99	E
PZE-101182888	1	231,208,427	9.34E-05	5.05	B, C
PZE-101188800	1	237,883,989	5.74E-04	0.92	D
PZE-101224367	1	279,939,641	3.43E-04	1.09	A
PZE-101233856	1	286,821,902	2.85E-04	3.93	B, C
PZE-102000560	2	837,383	5.60E-04	0.11	B, C
SYN4735	2	9,618,618	1.02E-05	5.08	B, E
SYN19565	2	32,086,278	1.84E-04	3.23	A
PZE-102055831	2	35,216,627	4.31E-04	1.15	A
PZA02450.1	2	49,124,335	5.70E-04	2.50	F
PZE-102082146	2	69,751,058	8.97E-04	4.28	F
SYN33606	2	169,623,783	4.00E-06	0.21	F
PZE-102123716	2	176,643,239	9.36E-05	2.66	D, F
PZE-102131295	2	187,143,781	3.36E-04	1.68	B
PZA03527.1	3	5,148,837	7.57E-04	7.09	B, C
PZE-103024939	3	16,957,568	1.76E-04	1.30	A
PZE-103065358	3	105,359,736	9.15E-07	1.97	A
PZE-103112971	3	175,092,704	6.95E-05	0.19	F
PZE-103165581	3	218,640,885	2.34E-05	5.86	E, F
PZE-104044786	4	69,044,273	1.14E-04	0.47	A
PZE-104080388	4	158,252,821	3.53E-05	0.01	A
PZE-104092771	4	171,771,502	5.79E-06	3.12	E
PZE-104116111	4	196,212,782	2.20E-04	2.78	E
SYN37141	4	227,482,564	3.12E-04	1.17	E
PZE-105024985	5	12,912,185	4.13E-04	2.10	B, F
SYN27691	5	23,539,045	2.36E-05	0.13	F
PZE-105070840	5	77,119,846	4.46E-04	0.60	A
PZE-105111323	5	172,217,865	1.39E-04	2.36	B, E
PZE-105132778	5	194,317,312	1.53E-04	0.96	C, F
PZE-105158980	5	212,371,623	6.15E-07	0.11	C
SYN35254	5	218,593,404	1.48E-04	2.71	B
PZE-106041751	6	93,712,294	3.59E-06	6.34	B, D, F
PZE-106041753	6	93,713,273	5.79E-06	6.56	C, E
PZE-106049962	6	102,943,268	1.07E-04	3.99	A
PZE-106049961	6	102,943,378	1.70E-04	3.60	C
SYN4597	6	107,195,543	1.11E-04	3.71	F
PZE-106088503	6	150,161,584	5.29E-04	1.77	E
PZE-106104150	6	159,598,074	1.94E-04	0.25	B
SYN4194	6	162,814,863	2.76E-05	2.98	B, C
SYN10687	6	169,009,504	4.06E-05	0.56	E
SYN32203	7	8,799,859	2.50E-05	0.02	D
SYN34669	7	9,820,060	5.57E-05	5.43	D, E
PZE-107044349	7	91,690,556	6.53E-04	0.08	B
SYN17951	7	143,619,654	3.39E-06	5.55	D, E, F
PZE-107088998	7	148,971,333	3.54E-05	0.10	E, F
SYN34204	7	156,490,174	8.51E-04	0.96	B
PZE-108005623	8	5,939,105	8.88E-05	3.99	A, D
PZE-108038271	8	63,280,888	5.15E-04	0.31	C
PZE-108053763	8	97,541,328	1.09E-07	0.03	D, F
SYN21795	8	117,579,482	7.45E-05	5.59	B, C
PZE-108064353	8	117,743,973	1.29E-04	2.07	F
ZM012274-0351	8	120,522,562	8.98E-05	2.03	E
SYN14914	8	132,971,220	6.87E-05	0.48	D
PZE-108078728	8	138,559,450	9.03E-04	2.54	B
PZE-109003046	9	3,291,982	5.83E-04	1.73	B, C
PZA03595.2	9	96,808,133	7.94E-05	0.70	F
PZE-109054725	9	98,196,277	7.53E-04	0.97	B
PZE-109069969	9	117,528,657	1.98E-04	1.15	A
SYN12403	10	2,241,835	1.30E-06	2.31	F
PZE-110061626	10	117,865,752	9.07E-07	0.67	A, C

附表1

表3

玉米籽粒淀粉含量显著相关SNP和候选基因功能注释"

关联位点 Associated SNP	染色体 Chr.	位置 Position (bp)	P值 P-value	表型变异率 PVE (%)	性状及环境 Trait and environment	候选基因 Candidate gene ID	基因名 Gene name	功能注释 Gene annotation	GO术语 GO term ID
PZE-101060842	1	44,730,532	4.27E-05	2.89	E, F^*	Zm00001d028735	Imd1	Isopropylmalate dehydrogenase1
						Zm00001d028737		Glucuronoxylan 4-O-methyltransferase 2	GO:0016051 GO:0034637 GO:0033692
PZE-101107894	1	115,245,510	4.01E-07	2.86	A, C, D, F	Zm00001d030236		Gibberellin-regulated protein 12
PZE-101182888	1	231,208,427	9.34E-05	5.05	B, C	Zm00001d032577	CESA4	CESA4 (CELLULOSE SYNTHASE A4)	GO:0016051 GO:0034637 GO:0033692
						Zm00001d032578	Dof13	C2C2-Dof-transcription factor 13
PZE-101233856	1	286,821,902	2.85E-04	3.93	B, C	Zm00001d034212	Hb8	Homeobox-transcription factor 8
PZE-102000560	2	837,383	5.60E-04	0.11	B, C	Zm00001d001785		C2 calcium/lipid-binding plant phosphoribosyltransferase family protein
						Zm00001d001791		Glucan endo-1,3-beta-D-glucosidase
SYN4735	2	9,618,618	1.02E-05	5.08	B, E	Zm00001d002285	NAC22	NAC-transcription factor 22
						Zm00001d002288	bHLH148	bHLH-transcription factor 148
						Zm00001d002292	Gpm461b	NAD(P)-binding Rossmann-fold superfamily protein	GO:0016051 GO:0034637 GO:0033692
PZE-102123716	2	176,643,239	9.36E-05	2.66	D, F	Zm00001d005502		Protein SMG7
						Zm00001d005506
PZA03527.1	3	5,148,837	7.57E-04	7.09	B, C	Zm00001d039469	Traf21	TNF receptor-associated factor 21
						Zm00001d039475	Mybr22	MYB-related-transcription factor 22
PZE-103165581	3	218,640,885	2.34E-05	5.86	E, F	Zm00001d044081	Hb46	Homeobox-transcription factor 46
						Zm00001d044083	Pin10	PIN-formed protein10
						Zm00001d044086		Nucleic acid-binding OB-fold-like protein
PZE-105024985	5	12,912,185	4.13E-04	2.10	B, F	Zm00001d013500		C2H2-type domain-containing protein
						Zm00001d013507		Heat shock 70 kDa protein 6 chloroplastic
PZE-105111323	5	172,217,865	1.39E-04	2.36	B, E	Zm00001d016674	HSF6	HSF-transcription factor 6
						Zm00001d016675	CTR1	Constitutive triple response1
						Zm00001d016684	Ae1	Amylose extender1	GO:0016051 GO:0034637 GO:0033692
PZE-105132778	5	194,317,312	1.53E-04	0.96	C, F	Zm00001d017391		Axial regulator YABBY 1
PZE-106041751	6	93,712,294	3.59E-06	6.34	B, D, F	Zm00001d036583		BEACH domain-containing protein C2
PZE-106041753	6	93,713,273	5.79E-06	6.56	C, E	Zm00001d036583		BEACH domain-containing protein C2
SYN4194	6	162,814,863	2.76E-05	2.98	B, C	Zm00001d038693	Dof10	C2C2-Dof-transcription factor 10
						Zm00001d038699		O-methyltransferase ZRP4
SYN34669	7	9,820,060	5.57E-05	5.43	D, E	Zm00001d018936		Ribose-5-phosphate isomerase	GO:0016051
						Zm00001d018937		MMS19 nucleotide excision repair protein
						Zm00001d018941	HSF4	HSF-transcription factor 4
SYN17951	7	143,619,654	3.39E-06	5.55	D, E, F	Zm00001d021129		Alpha-(14)-fucosyltransferase	GO:0016051 GO:0034637 GO:0033692
						Zm00001d021130
						Zm00001d021135	Pebp24	Phosphatidylethanolamine-binding protein24
						Zm00001d021136	PTI3	Like tyrosine-protein kinase 3
PZE-107088998	7	148,971,333	3.54E-05	0.10	E, F	Zm00001d021325		L-Aspartase-like family protein
PZE-108005623	8	5,939,105	8.88E-05	3.99	A, D	Zm00001d008338	Trps14	Trehalose-6-phosphate synthase14	GO:0016051 GO:0034637
						Zm00001d008345		Importin subunit alpha
PZE-108053763	8	97,541,328	1.09E-07	0.03	D, F	Zm00001d010056		Delta-1-pyrroline-5-carboxylate synthase
						Zm00001d010059		KH domain-containing protein
SYN21795	8	117,579,482	7.45E-05	5.59	B, C	Zm00001d010487		UDP-glycosyltransferase 88A1
						Zm00001d010490		CW-type Zinc Finger
PZE-109003046	9	3,291,982	5.83E-04	1.73	B, C	Zm00001d044812	Pin1	PIN-formed protein1
						Zm00001d044813	Gpm441	Putative fructokinase-6 chloroplastic	GO:0016051 GO:0034637 GO:0033692
PZE-110061626	10	117,865,752	9.07E-07	0.67	A, C	Zm00001d025409	Ereb21	Putative AP2/EREBP transcription factor superfamily protein
						Zm00001d025412		Nicotinate phosphoribosyltransferase

表3

附图3

图2

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性状及环境 Trait and environment	变异范围 Range (%)	平均值 Average (%)	标准差 SD	变异系数 CV (%)	偏度 Skewness	峰度 Kurtosis
WSYC2019	61.46-71.16	66.95	1.62	2.42	-0.40	-0.03
WSPG2020	59.66-68.94	64.55	1.57	2.43	-0.17	-0.29
DSYC2019	68.14-75.97	72.59	1.21	1.67	-0.49	0.64
DSPG2020	66.40-75.22	71.19	1.27	1.78	-0.25	0.14

性状及环境 Trait and environment	相关系数Correlation coefficient
性状及环境 Trait and environment	WSYC2019	WSPG2020	DSYC2019	DSPG2020
WSYC2019	1
WSPG2020	0.627^**	1
DSYC2019	0.804^**	0.526^**	1
DSPG2020	0.563^**	0.844^**	0.610^**	1

玉米籽粒淀粉含量全基因组关联分析和候选基因预测

Genome-wide association study and candidate gene prediction of kernel starch content in maize

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