玉米花期根系结构的表型变异与全基因组关联分析

doi:10.3864/j.issn.0578-1752.2019.14.002

Abstract

Abstract:

【Objective】The root system as an important organ absorbing water and nutrients for plants, is essential for growth and grain yield of maize. More understanding of the genetic mechanism of the root architecture of maize is of great significance for the practice of high-yield breeding of maize.【Method】In this study, 111 maize elite inbred lines were used as an association population. In 2017, six belowground nodal root-related traits, i.e. nodal root layer number (RLN), total nodal root number (TRN), nodal root angle (RA), nodal root area (RS), nodal root volume (RV) and nodal root dry weight (RDW), were measured under four environments including Beijing, Yongshou of Shanxi province, Dingxiang of Shanxi province and Yuanyang of Henan province. The average of the four environments were used as the phenotypic data of the six root-related traits. The statistical analysis and correlation analysis were carried out on six traits, and the differences of six root-related traits for inbred lines developed in different eras and for inbred lines in different heterotic groups were also analyzed. Based on 152352 high-quality SNP markers obtained in this population, the FarmCPU model was used for genome-wide association analysis to obtain significantly associated SNP loci, and candidate genes were predicted based on the LD interval sequence of these significant associated SNPs, and a functional enrichment analysis of candidate genes was carried out.【Result】The phenotypic analysis showed that the six belowground nodal root traits exhibited a normal distribution and high level of heritability. The correlation analysis showed that RLN and TRN are negatively correlated with RA and RS; RA, RS, RV and RDW are significantly positively correlated with each other. With the advance of maize breeding era, RLN and TRN had a decreasing trend, and RA and RS had an increasing trend. There were no significant differences for RDW and RV among inbred lines of different eras. The belowground root structure of those inbred lines from different maize heterotic groups also showed differences, and the six traits of the Lüda Red Cob group were all higher than those of other groups. Genome-wide association study (GWAS) yielded 26 significantly associated SNPs (P<0.00001) referring to RLN, TRN, RV and RDW, of which 11 SNPs located in root-related QTLs previously reported, and 2 SNPs were detected to be significant correlation with RLN and TRN. A total of 177 candidate genes were found based on those significantly associated SNPs, of which 135 genes have functional annotation, the gene Zm00001d037368 was one pleiotropic gene influencing RLN and TRN. The results of enrichment analysis of candidate genes mainly involved in metabolic regulation, the response to stress, transporter activity, catalytic activity, binding protein and cellular components in plants.【Conclusion】The root architecture of maize inbred lines from different eras and different heterotic groups had differences with various degree. Root-related genetic loci and candidate genes identified by the genome-wide association analysis, a total of 26 loci associated with root-related traits were identified.

Key words: maize (Zea mays L.), nodal root, genome-wide association study, candidate gene

ZHANG XiaoQiong,GUO Jian,DAI ShuTao,REN Yuan,LI FengYan,LIU JingBao,LI YongXiang,ZHANG DengFeng,SHI YunSu,SONG YanChun,LI Yu,WANG TianYu,ZOU HuaWen,LI ChunHui. Phenotypic Variation and Genome-wide Association Analysis of Root Architecture at Maize Flowering Stage[J].Scientia Agricultura Sinica, 2019, 52(14): 2391-2405.

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Figures/Tables 12

Fig. 1

Table 1

Fig. 2

Table 2

Fig. 3

Fig. 4

Table 3

Statistical analysis of belowground nodal root-related traits in inbred lines of different heterotic groups"

性状/类群 Trait/Group	均值 Mean	标准差 SD	极小值 Min	极大值 Max	变异系数 CV (%)
RLN
瑞德Reid	6.47ab	0.64	5.38	8.22	9.94
旅大红骨LRC	6.86a	0.56	6.17	8.00	8.13
兰卡斯特Lancaster	6.44b	0.43	5.56	7.33	6.73
塘四平头TSPT	7.02a	0.64	6.17	8.17	9.12
P群P group	6.54ab	0.52	5.83	7.21	7.92
混合群Mixed group	7.08a	0.55	6.33	8.67	7.76
TRN
瑞德Reid	56.86b	7.33	43.13	75.83	12.90
旅大红骨LRC	63.72a	10.53	49.39	77.33	16.52
兰卡斯特Lancaster	55.83b	6.51	42.00	68.67	11.66
塘四平头TSPT	63.79a	10.47	48.11	86.67	16.41
P群P group	60.40ab	9.26	47.92	74.80	15.33
混合群Mixed group	63.35a	9.77	51.67	88.00	15.42
RA
瑞德Reid	61.32a	7.13	48.65	80.70	11.62
旅大红骨LRC	62.66a	4.81	53.71	67.65	7.67
兰卡斯特Lancaster	58.43ab	9.82	43.89	78.03	16.81
塘四平头TSPT	54.82b	6.94	44.87	66.00	12.66
P群P group	57.52ab	8.23	43.71	67.99	14.31
混合群Mixed group	55.76ab	9.94	35.82	71.87	17.82
RS
瑞德Reid	82.07a	11.62	60.58	109.61	14.16
旅大红骨LRC	82.68a	12.71	68.47	106.65	15.37
兰卡斯特Lancaster	74.90a	14.99	48.38	111.91	20.02
塘四平头TSPT	65.50b	10.22	51.80	88.01	15.60
P群P group	73.68ab	13.88	57.50	97.73	18.84
混合群Mixed group	74.34a	13.85	45.55	107.94	18.63
RV
瑞德Reid	69.72ab	23.36	34.21	140.83	33.51
旅大红骨LRC	81.82a	33.68	38.31	144.17	41.17
兰卡斯特Lancaster	66.95ab	23.85	19.63	124.52	35.63
塘四平头TSPT	71.59ab	29.86	33.33	139.17	41.71
P群P group	68.97ab	24.45	44.37	107.99	35.45
混合群Mixed group	60.62b	19.36	38.33	123.11	31.93
RDW
瑞德Reid	14.25a	4.34	6.49	24.86	30.44
旅大红骨LRC	16.21a	7.84	7.55	32.60	48.38
兰卡斯特Lancaster	13.07a	4.92	4.09	28.32	37.68
塘四平头TSPT	12.26a	4.99	5.21	25.07	40.66
P群P group	14.22a	4.60	8.99	23.49	32.35
混合群Mixed group	13.74a	5.55	5.86	31.29	40.41

Table 3

Fig. 5

Fig. 6

Table 4

List of significant SNPs affecting maize belowground nodal root-related traits and the plausible candidate genes and their functional annotations"

性状 Trait	SNP	Chr.	位置^a Position (bp)	P值 P value	候选基因^b Candidate gene	基因功能注释 Gene annotation	参考文献^c Reference
RLN	Chr.1.S_31312069	1	31312069	3.07E-06	Zm00001d028337	富含脯氨酸的受体样蛋白激酶PERK4 Proline-rich receptor-like protein kinase PERK4
RLN	Chr.1.S_31312087	1	31312087	3.07E-06	Zm00001d028344	推定的金属耐受蛋白C3 Putative metal tolerance protein C3
RDW	Chr.3.S_103120493	3	103120493	1.07E-05	Zm00001d041183	蛋白激酶超家族蛋白质/苏氨酸蛋白激酶prpf4B-liken Protein kinase superfamily proteiserine/threonine-protein kinase prpf4B-liken
RV	Chr.3.S_104251070	3	104251070	8.33E-06	Zm00001d041192	蔗糖转运蛋白4 Sucrose transporter4
RDW	Chr.4.S_9975093	4	9975093	7.24E-06	Zm00001d048943	硫氧还蛋白超家族蛋白 Thioredoxin superfamily protein	[14]
RV	Chr.4.S_38214896	4	38214896	3.38E-06	Zm00001d049623	SNARE相关蛋白 SNARE-associated protein-related
					Zm00001d049627	蛋氨酸氨肽酶 Methionine aminopeptidase
RV	Chr.4.S_63797065	4	63797065	7.79E-06	Zm00001d050069	海藻糖-6-磷酸合成酶8 Trehalose-6-phosphate synthase8
RV	Chr.4.S_100804613	4	100804613	8.30E-06	Zm00001d050558	OSJNBa0043A12.20蛋白 OSJNBa0043A12.20 protein
TRN	Chr.4.S_246664102	4	246664102	3.96E-06	Zm00001d054104	E3泛素蛋白连接酶UPL3 E3 ubiquitin-protein ligase UPL3
					Zm00001d054105	尿苷激酶样蛋白3 Uridine kinase-like protein 3
RDW	Chr.6.S_34950886	6	34950886	9.19E-06	Zm00001d035587	G型凝集素S受体样丝氨酸/苏氨酸蛋白激酶At2g19130 G-type lectin S-receptor-like serine/threonine-protein kinase At2g19130	[5,20]
					Zm00001d035588	G型凝集素S受体样丝氨酸/苏氨酸蛋白激酶At2g19130 G-type lectin S-receptor-like serine/threonine-protein kinase At2g19130
RDW	Chr.6.S_108781517	6	108781517	6.09E-07	Zm00001d037004	Ras相关蛋白RABA1d Ras-related protein RABA1d	[17]
					Zm00001d037010	毛发相关蛋白激酶iota Shaggy-related protein kinase iota
RLN/TRN	Chr.6.S_123079904	6	123079904	4.00E-06	Zm00001d037360	推定的bZIP转录因子超家族蛋白 Putative bZIP transcription factor superfamily protein	[20]
RLN/TRN	Chr.6.S_123079927	6	123079927	4.00E-06	Zm00001d037368	未知 Unknown	[20]
RLN	Chr.6.S_123845438	6	123845438	2.51E-06	Zm00001d037384	花青素3-O-葡糖基转移酶 Anthocyanidin 3-O-glucosyltransferase	[20]
TRN	Chr.6.S_135051799	6	135051799	6.13E-06	Zm00001d037712	MAR结合丝状蛋白1 MAR-binding filament-like protein 1
RV	Chr.6.S_136591446	6	136591446	6.19E-06	Zm00001d037751	晚期胚胎发育丰富（LEA）富含羟脯氨酸的糖蛋白家族 Late embryogenesis abundant (LEA) hydroxyproline-rich glycoprotein family
RDW	Chr.7.S_48142656	7	48142656	3.42E-06	Zm00001d019648	核酸结合蛋白1 Nucleic acid binding protein 1	[14]
RDW	Chr.7.S_101804639	7	101804639	7.71E-07	Zm00001d020242	锌指CCCH结构域的蛋白质64 Zinc finger CCCH domain-containing protein 64	[14]
RLN	Chr.8.S_55681954	8	55681954	5.47E-06	Zm00001d009324	AMSH样泛素蛋白硫酯酶3 AMSH-like ubiquitin thioesterase 3
RV	Chr.8.S_100196991	8	100196991	1.68E-06	Zm00001d010119	冷休克蛋白CS66 Cold shock protein CS66	[20]
RV	Chr.8.S_100680141	8	100680141	1.07E-07	Zm00001d010128	酸性核糖体蛋白P2b（rpp2b） Acidic ribosomal protein P2b (rpp2b)	[20]
RV	Chr.9.S_67485696	9	67485696	3.82E-07	Zm00001d046152	推定的RING-H2指蛋白ATL71 Putative RING-H2 finger protein ATL71
RV	Chr.9.S_111860806	9	111860806	9.44E-06	Zm00001d046942	果糖-1,6-二磷酸酶 Fructose-1,6-bisphosphatase
RV	Chr.10.S_150110617	10	150110617	1.08E-05	Zm00001d026687	生长素响应因子17 Auxin response factor 17	[14]
					Zm00001d026694	生长素响应因子13 Auxin response factor 13

Table 4

Fig. 7

Fig. 8

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性状 Trait	均值 Mean	最大值 Max	最小值 Min	标准差 SD	变异系数 CV (%)	广义遗传力 H²
地下节根层数RLN	6.67	8.67	5.38	0.62	9.29	0.67
地下节根总条数TRN	59.41	88.00	42.00	8.96	15.08	0.74
地下节根角度RA	58.67	80.70	35.82	8.51	14.50	0.80
地下节根面积RS	76.28	111.91	45.55	13.85	18.15	0.79
地下节根体积RV	68.75	144.17	19.63	24.84	36.13	0.75
地下节根干重RDW	13.77	32.60	4.09	5.11	37.12	0.82

年代 Era	材料数量 Number of materials	材料名称 Name of materials
1970s	10	C103、E28、H21、Mo17、丹黄02 Danhuang02、黄早四Huangzaosi、威风322 Weifeng322、掖8112 Ye8112、原武02 Yuanwu02、吉63 Ji63
1980s	17	853、5003、81162、4F1、B73、K12、Mo17Ht、X178、丹340 Dan340、合344 He344、齐319 Qi319、天涯4 Tianya4、铁7922 Tie7922、掖478 Ye478、掖488 Ye488、掖52106 Ye52106、郑58 Zheng58
1990s	14	444、5237、A801、C8605-2、Ki3、KL4、P138、昌7-2 Chang7-2、丹598 Dan598、多229 Duo229、黄野四3 Huangyesi3、获唐黄17 Huotanghuang17、沈137 Shen137、郑22 Zheng22
2000s	5	沈3336 Shen3336、四-144 Si-144、PH6JM、京724 Jing724、京725 Jing725

Phenotypic Variation and Genome-wide Association Analysis of Root Architecture at Maize Flowering Stage

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