玉米叶绿素含量的全基因组关联分析

doi:10.3864/j.issn.0578-1752.2019.11.001

Abstract

Abstract:

【Objective】 Chlorophyll content was positively correlated with crop yield, improving crop yield by increasing chlorophyll content has become an important breeding goal in maize. Thus, elucidating the genetic basis of chlorophyll content using genome-wide association study (GWAS) can provide theoretical support for ideotype-based maize breeding with high photosynthetic efficiency. 【Method】 The association mapping panel (AMP) used in this study was consisted of 538 maize inbred lines, chlorophyll content of maize three leaves (above the uppermost ear leaf, uppermost ear leaf and below the uppermost ear leaf ) of the AMP was investigated at 5 days after pollination at five locations, then a GWAS with three models (Q, K, Q+K) were carried out using 558 629 single nucleotide polymorphisms (SNPs). The combination of optimal GWAS model with expression quantitative trait loci (eQTL) analysis, natural variation of chlorophyll content was further explored. 【Result】 All traits measured at the five locations exhibited an approximately normal distribution and positive correlations between paired traits were also observed. Analysis of variance indicated that significant variations were observed across environment, genotype and the genotype × environment interaction. In addition, the heritability of chlorophyll content was 0.66, 0.66, and 0.67 for above the uppermost ear leaf, uppermost ear leaf and below the uppermost ear leaf, respectively. When test with the optimal GWAS model, K model has the greatest success in reducing false positive (type I errors) than other two models. Based on the result of K model, a total of 18 loci involving in 29 significantly SNP-traits associations were detected (P≤3.99×10 ^-6), and 76 candidate genes were found, including 42 genes that have functional annotation that involved in energy metabolism, biosynthetic regulation and material transportation and metabolic pathways. Of which, 85.5% (65/76) of the candidate genes have eQTLs and 11.8% (9/76) of the candidate genes were significantly associated with the corresponding phenotype (P＜0.05), indicating that these nine genes may affect phenotypic variation by regulating their expression. Moreover, two loci were found to be co-localized in two environments or leaves, the gene GRMZM2G074759 within the co-localized locus, encodes an acyl-activating enzyme, highly similar to AAE3. It can increase the lysine content and improve maize quality by increasing the content of α-ketoglutarate (ALA) and oxaloacetate, in addition, ALA could promote chlorophyll biosynthesis and improve crop yield, this gene was considered as the most likely candidate gene. 【Conclusion】 The results indicated that K model having the best result in reducing the false positive. Based on the K model, a total of 18 loci associated with chlorophyll content and several candidate genes may be involved in chlorophyll synthesis pathway were identified.

Key words: maize (Zea mays L.), chlorophyll content, genome-wide association study, high photosynthetic efficiency

SHI DaKun, YAO TianLong, LIU NanNan, DENG Min, DUAN HaiYang, WANG LuLin, WAN Jiong, GAO JiongHao, XIE HuiLing, TANG JiHua, ZHANG XueHai. Genome-Wide Association Study of Chlorophyll Content in Maize[J].Scientia Agricultura Sinica, 2019, 52(11): 1839-1857.

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https://www.chinaagrisci.com/EN/Y2019/V52/I11/1839

Figures/Tables 6

Table 1

Fig. 1

Table 2

Fig. 2

Fig. 3

Table 3

Candidate genes and their annotation of chlorophyll content in maize three ear leaves at six environments"

位点^a Loci	染色 Chr.	环境 Enviro.	性状 Trait	峰值SNP Peak SNP	物理位置^b Posi. (bp)	P值^c P value	贡献率^d R²(%)	候选基因^e Candidate gene	功能注释 Annotation
1	1	2018年长沙 Changsha, 2018	穗位叶 Uppermost ear leaf	Chr.1.S_33879839	33879839	1.05E-06	5.89	GRMZM2G110023	ATP结合亚基CLPT1叶绿体 ATP-dependent Clp protease ATP-binding subunit CLPT1 chloroplastic
								GRMZM2G110004	NA
								GRMZM2G035552	ACR8
								GRMZM2G035461	自噬蛋白9Autophagy protein 9
2	1	2017年三亚 Sanya, 2017	穗位叶 Uppermost ear leaf	Chr.1.S_249417295	249417295	2.65E-06	5.43	GRMZM2G031771	NA
								GRMZM2G031788	NA
								GRMZM2G058057	同源线粒体导入受体亚基 Mitochondrial import receptor subunit TOM5 homolog TOM5
								GRMZM2G058227	甘油磷酰二元酸酯磷酸二酯酶Glycerophosphoryl diester phosphodiesterase
								GRMZM2G058244	UDP -葡萄糖6脱氢酶UDP-glucose 6-dehydrogenase
								GRMZM2G172512	未知Unknown
								GRMZM2G172584	未知Unknown
2	1	2017年三亚 Sanya, 2017	穗位叶 Uppermost ear leaf	Chr.1.S_249417300	249417300	2.65E-06	5.43	GRMZM2G031771	NA
								GRMZM2G031788	NA
								GRMZM2G058057	TOM5同源线粒体导入受体亚基 Mitochondrial import receptor subunit TOM5 homolog
								GRMZM2G058227	甘油磷酰二元酸酯磷酸二酯酶Glycerophosphoryl diester phosphodiesterase
								GRMZM2G058244	UDP -葡萄糖6脱氢酶UDP-glucose 6-dehydrogenase
								GRMZM2G172512	未知Unknown
								GRMZM2G172584	未知Unknown
2	1	2017年三亚 Sanya, 2017	穗位叶 Uppermost ear leaf	Chr.1.S_249417301	249417301	2.65E-06	5.43	GRMZM2G031771	NA
								GRMZM2G031788	NA
								GRMZM2G058057	TOM5同源线粒体导入受体亚基 Mitochondrial import receptor subunit TOM5 homolog
								GRMZM2G058227	甘油磷酰二元酸酯磷酸二酯酶Glycerophosphoryl diester phosphodiesterase
								GRMZM2G058244	UDP -葡萄糖6脱氢酶UDP-glucose 6-dehydrogenase
位点^a Loci	染色 Chr.	环境 Enviro.	性状 Trait	峰值SNP Peak SNP	物理位置^b Posi. (bp)	P值^c P value	贡献率^d R²(%)	候选基因^e Candidate gene	功能注释 Annotation
								GRMZM2G172512	未知Unknown
								GRMZM2G172584	未知Unknown
3	3	2012年鹤壁 Hebi, 2012	穗下叶Below the uppermost ear leaf	Chr.3.S_167437401	167437401	2.88E-07	6.52	GRMZM2G701895	NA
								GRMZM2G044055	甲酸精蛋白1Formin-like protein 1
								GRMZM2G044092	葡萄糖苷酶42Beta-glucosidase 42
								GRMZM2G118362	含五肽复合物的线粒体蛋白 Pentatricopeptide repeat-containing protein mitochondrial
4	3	综合Blup	穗上叶Above the uppermost ear leaf	PZE-103136749	192318356	6.48E-07	5.10	GRMZM2G038953	54 kD蛋白3信号识别粒子Signal recognition particle 54 kD protein 3
5	5	综合Blup	穗上叶Above the uppermost ear leaf	PZE-105049606	41552842	1.46E-06	4.80	GRMZM2G007185	β13-半乳糖基转移酶4 Probable beta-13-galactosyltransferase 4
5	5	综合Blup	穗上叶Above the uppermost ear leaf	PZE-105049607	41552873	2.58E-06	4.53	GRMZM2G007185	β13-半乳糖基转移酶4 Probable beta-13-galactosyltransferase 4
6	5	2012年鹤壁 Hebi, 2012	穗位叶 Uppermost ear leaf	Chr.5.S_174139937	174139937	2.23E-06	5.36	GRMZM5G836353	单氧酶1 Monooxygenase 1
								GRMZM2G339523	单氧酶1 Monooxygenase 1
								GRMZM2G087169	单氧酶1 Monooxygenase 1
								GRMZM2G087068	类Cmc1细胞色素c氧化酶生物发生蛋白 Cytochrome c oxidase biogenesis protein Cmc1-like
								GRMZM2G388099	未知Unknown
								GRMZM2G087040	乙烯反应转录因子ERF021Ethylene-responsive transcription factor ERF021
								GRMZM2G086946	TPX2（靶向蛋白为Xklp2）蛋白家族 TPX2 (targeting protein for Xklp2) protein family
7	5	综合Blup	穗下叶Below the uppermost ear leaf	Chr.5.S_216586758	216586758	2.75E-06	5.03	GRMZM2G014116	26S蛋白酶体非ATP酶调节亚基 26S proteasome non-ATPase regulatory subunit 12 homolog B
								GRMZM2G014793	O-岩藻糖转移酶家族蛋白O-fucosyltransferase family protein
								GRMZM2G015090	植物细胞内ras -group相关LRR蛋白 Plant intracellular Ras-group-related LRR protein 9
								GRMZM2G145061	脯氨酰4羟化酶亚基α2 Prolyl 4-hydroxylase alpha-2 subunit
								GRMZM2G145107	蔗糖转运2 Sucrose transporter2
								GRMZM2G145128	含有重复PPR的线粒体蛋白Pentatricopeptide repeat-containing protein
位点^a Loci	染色 Chr.	环境 Enviro.	性状 Trait	峰值SNP Peak SNP	物理位置^b Posi. (bp)	P值^c P value	贡献率^d R²(%)	候选基因^e Candidate gene	功能注释 Annotation
								GRMZM2G145133	未知Unknown
								GRMZM2G445944	转录因子TCP21Transcription factor TCP21
								GRMZM2G445958	复制蛋白a32 kD亚基A Replication protein A 32 kD subunit A
								GRMZM2G145473	未知Unknown
8	7	2012年鹤壁 Hebi, 2012	穗下叶Below the uppermost ear leaf	Chr.7.S_9204823	9204823	4.39E-07	6.37	GRMZM2G704349	Pumilio同源3 Pumilio homolog 3
								GRMZM2G046776	Pumilio同源3 Pumilio homolog 3
								GRMZM2G046750	脂质转运蛋白Lipid-transfer protein 种子贮藏2S白蛋白超家族蛋白Seed storage 2S albumin superfamily protein
								GRMZM2G046529	叶绿体中蛋白质脂肪酸输出1 Protein FATTY ACID EXPORT 1 chloroplastic
								GRMZM2G004301	Ⅳ型肌醇多磷酸酶Type Ⅳ inositol polyphosphate
9	7	2017年三亚 Sanya, 2017	穗下叶Below the uppermost ear leaf	Chr.7.S_145681493	145681493	1.72E-06	5.54	GRMZM2G168913	RNA聚合酶Ⅱ的中介体亚单位8 Mediator of RNA polymerase Ⅱtranscription subunit 8
								GRMZM2G168858	NADPH-细胞色素P450还原酶NADPH--cytochrome P450 reductase 2
								GRMZM2G357688	锌指蛋白2 Zinc finger protein 2
								GRMZM2G436511	BTB/POZ蛋白域 BTB/POZ domain-containing protein
								GRMZM2G135651	环核苷酸封闭通道Cyclic nucleotide-gated ion channel 14
9	7	2017年三亚 Sanya, 2017	穗下叶Below the uppermost ear leaf	Chr.7.S_145682189	145682189	5.85E-07	6.07	GRMZM2G168913	RNA聚合酶Ⅱ的中介体亚单位8 Mediator of RNA polymeraseⅡ transcription subunit 8
								GRMZM2G168858	NADPH-细胞色素P450还原酶2 NADPH--cytochrome P450 reductase 2
								GRMZM2G357688	锌指蛋白2Zinc finger protein 2
								GRMZM2G436511	BTB/POZ蛋白域BTB/POZ domain-containing protein
								GRMZM2G135651	环核苷酸封闭通道Cyclic nucleotide-gated ion channel 14
10	8	2012年鹤壁 Hebi, 2012	穗上叶Above the uppermost ear leaf	Chr.8.S_1454124	1454124	1.32E-06	5.55	GRMZM2G378906	外被体蛋白β亚基Coatomer subunit beta
								GRMZM2G110368	未知Unknown
11	8	综合Blup	穗位叶 Uppermost ear leaf	Chr.8.S_1454124	1454124	3.95E-06	4.70	GRMZM2G378906	外被体蛋白β亚基Coatomer subunit beta
								GRMZM2G110368	未知Unknown
位点^a Loci	染色 Chr.	环境 Enviro.	性状 Trait	峰值SNP Peak SNP	物理位置^b Posi. (bp)	P值^c P value	贡献率^d R²(%)	候选基因^e Candidate gene	功能注释 Annotation
12	9	综合Blup	穗上叶Above the uppermost ear leaf	Chr.9.S_9638369	9638369	1.32E-06	4.86	GRMZM2G159402	假定锌指蛋白Putative zinc finger protein
								GRMZM2G033130	DUF1296结构域蛋白家族 Putative DUF1296 domain containing family protein
12	9	综合Blup	穗上叶Above the uppermost ear leaf	Chr.9.S_9639904	9639904	1.32E-06	4.86	GRMZM2G159402	假定锌指蛋白Putative zinc finger protein
								GRMZM2G033130	DUF1296结构域蛋白家族Putative DUF1296 domain containing family protein
12	9	综合Blup	穗上叶Above the uppermost ear leaf	chr9.S_9642472	9642472	1.32E-06	4.86	GRMZM2G159402	假定锌指蛋白Putative zinc finger protein
								GRMZM2G033130	DUF1296结构域蛋白家族Putative DUF1296 domain containing family protein
12	9	综合Blup	穗上叶Above the uppermost ear leaf	Chr.9.S_9643507	9643507	1.32E-06	4.86	GRMZM2G159402	假定锌指蛋白Putative zinc finger protein
								GRMZM2G033130	DUF1296结构域蛋白家族Putative DUF1296 domain containing family protein
12	9	综合Blup	穗上叶Above the uppermost ear leaf	Chr.9.S_9644832	9644832	1.32E-06	4.86	GRMZM2G159402	假定锌指蛋白Putative zinc finger protein
								GRMZM2G033130	DUF1296结构域蛋白家族Putative DUF1296 domain containing family protein
13	9	2017年三亚 Sanya, 2017	穗位叶 Uppermost ear leaf	Chr.9.S_151327393	151327393	1.72E-06	6.01	GRMZM2G178787	叶绿体蛋白激酶Protein kinase 2B chloroplastic
								GRMZM2G178826	脱氢奎尼酸合酶3-dehydroquinate synthase
								GRMZM2G479529	未知Unknown
								GRMZM2G178847	未知Unknown
								GRMZM2G178859	原血红素Ⅸ法氏转移酶Protoheme Ⅸ farnesyltransferase
								GRMZM2G178880	甘露聚糖合酶7 Probable mannan synthase 7
								GRMZM2G178916	含有重复PPR的线粒体蛋白 Pentatricopeptide repeat-containing protein mitochondrial
								GRMZM2G479581	未知Unknown
								GRMZM2G178945	O-岩藻糖转移酶家族蛋白O-fucosyltransferase family protein
								GRMZM2G178960	核酮糖磷酸3-表异构酶Ribulose-phosphate 3-epimerase
								GRMZM2G057950	核糖体蛋白L32含有蛋白质的异构体1%3B核糖体蛋白L32,含有蛋白质的异构体 2Ribosomal protein L32 containing protein isoform 1%3B, Ribosomal protein L32 containing protein isoform 2
位点^a Loci	染色 Chr.	环境 Enviro.	性状 Trait	峰值SNP Peak SNP	物理位置^b Posi. (bp)	P值^c P value	贡献率^d R²(%)	候选基因^e Candidate gene	功能注释 Annotation
								GRMZM2G058037	类HVA22蛋白Ⅰ HVA22-like proteinⅠ
								GRMZM2G361256	ATP结合盒（ABC)蛋白家族3 ABC transporter C family member 3
14	9	2017年三亚 Sanya, 2017	穗位叶 Uppermost ear leaf	Chr.9.S_153737236	153737236	7.91E-07	6.59	GRMZM2G382537	未知Unknown
								GRMZM2G382534	羟化酶5 Hydroxylase5
								GRMZM2G060564	PLAC8 家族蛋白PLAC8 family protein
								GRMZM2G060507	假定类结转录因子家族蛋白Putative knotted-like transcription factor family protein
								GRMZM2G064005	Protein FIZZY-RELATED 1 FIZZY-RELATED蛋白
								GRMZM2G063931	假定泛素连接酶酶家族,E2泛素连接酶 Putative ubiquitin-conjugating enzyme family%3B, ubiquitin-conjugating enzyme E2
15	10	2012年鹤壁 Hebi, 2012	穗位叶 Uppermost ear leaf	Chr.10.S_45404195	45404195	2.81E-06	4.76	NO	-
16	10	2012年鹤壁 Hebi, 2012	穗位叶 Uppermost ear leaf	Chr.10.S_46780569	46780569	2.76E-06	4.75	GRMZM2G135800	NA
								GRMZM2G371316	未知Unknown
								GRMZM2G371345	黄酮醇3-O-葡糖基转移酶Flavonol 3-O-glucosyltransferase
16	10	2012年鹤壁 Hebi, 2012	穗位叶 Uppermost ear leaf	Chr.10.S_46780652	46780652	2.76E-06	4.75	GRMZM2G135800	NA
								GRMZM2G371316	未知Unknown
								GRMZM2G371345	黄酮醇3-O-葡糖基转移酶Flavonol 3-O-glucosyltransferase
17	10	2018年长沙 Changsha, 2018	穗位叶 Uppermost ear leaf	Chr.10.S_148643242	148643242	3.04E-06	5.30	GRMZM2G074787	DNA错配修复蛋白MSH3 DNA mismatch repair protein MSH3
								GRMZM2G074773	核转录因子Y亚基C-4 Nuclear transcription factor Y subunit C-4
								GRMZM2G074759	酰基活化酶3 Acyl activating enzyme3
								GRMZM2G074754	C2钙/脂结合植物磷脂酰转移酶家族蛋白 C2 calcium/lipid-binding plant phosphoribosyltransferase family protein
								GRMZM2G074718	表达蛋白Expressed protein
								GRMZM2G074107	DNA结合蛋白DNA binding protein
位点^a Loci	染色 Chr.	环境 Enviro.	性状 Trait	峰值SNP Peak SNP	物理位置^b Posi. (bp)	P值^c P value	贡献率^d R²(%)	候选基因^e Candidate gene	功能注释 Annotation
17	10	2018年长沙 Changsha, 2018	穗位叶 Uppermost ear leaf	Chr.10.S_148643247	148643247	3.87E-06	5.27	GRMZM2G074787	DNA错配修复蛋白MSH3 DNA mismatch repair protein MSH3
								GRMZM2G074773	核转录因子Y亚基C-4 Nuclear transcription factor Y subunit C-4
								GRMZM2G074759	酰基活化酶3 Acyl activating enzyme3
								GRMZM2G074754	C2钙/脂结合植物磷脂酰转移酶家族蛋白 C2 calcium/lipid-binding plant phosphoribosyltransferase family protein
								GRMZM2G074718	表达蛋白Expressed protein
								GRMZM2G074107	DNA结合蛋白DNA binding protein
17	10	2018年长沙 Changsha, 2018	穗位叶 Uppermost ear leaf	Chr.10.S_148643249	148643249	1.78E-07	6.71	GRMZM2G074787	DNA错配修复蛋白MSH3 DNA mismatch repair protein MSH3
								GRMZM2G074773	核转录因子Y亚基C-4 Nuclear transcription factor Y subunit C-4
								GRMZM2G074759	酰基活化酶3 Acyl activating enzyme3
								GRMZM2G074754	C2钙/脂结合植物磷脂酰转移酶家族蛋白 C2 calcium/lipid-binding plant phosphoribosyltransferase family protein
								GRMZM2G074718	表达蛋白Expressed protein
								GRMZM2G074107	DNA结合蛋白DNA binding protein
18	10	2018年长沙 Changsha, 2018	穗上叶Above the uppermost ear leaf	Chr.10.S_148643249	148643249	1.58E-06	5.80	GRMZM2G074787	DNA错配修复蛋白MSH3 DNA mismatch repair protein MSH3
								GRMZM2G074773	核转录因子Y亚基C-4 Nuclear transcription factor Y subunit C-4
								GRMZM2G074759	酰基活化酶3 Acyl activating enzyme3
								GRMZM2G074754	C2钙/脂结合植物磷脂酰转移酶家族蛋白 C2 calcium/lipid-binding plant phosphoribosyltransferase family protein
								GRMZM2G074718	表达蛋白Expressed protein
								GRMZM2G074107	DNA结合蛋白DNA binding protein

Table 3

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环境 Environment	性状 Traits	变异范围 Range	均值 Mean	标准差 sd.	偏度 Ske.	峰度 Kur.
2012年鹤壁Hebi, 2012	穗上叶Above the uppermost ear leaf	26.25—67.85	52.98	6.91	-0.87	1.51
	穗位叶Uppermost ear leaf	22.25—68.60	52.82	7.17	-0.97	1.69
	穗下叶Below the uppermost ear leaf	18.25—66.20	52.92	7.58	-1.08	1.92
2017年三亚Sanya, 2017	穗上叶Above the uppermost ear leaf	29.25—68.45	50.97	6.39	-0.46	0.90
	穗位叶Uppermost ear leaf	25.83—70.45	51.08	6.37	-0.43	1.16
	穗下叶Below the uppermost ear leaf	25.65—69.60	51.03	6.67	-0.48	0.92
2018年长沙Changsha, 2018	穗上叶Above the uppermost ear leaf	27.90—82.93	53.84	6.20	-0.26	3.08
	穗位叶Uppermost ear leaf	29.47—82.95	53.83	6.10	-0.08	2.98
	穗下叶Below the uppermost ear leaf	22.88—95.28	53.93	7.44	-0.09	4.59
2018年原阳Yuanyang, 2018	穗上叶Above the uppermost ear leaf	30.80—63.35	48.05	5.74	-0.48	0.97
	穗位叶Uppermost ear leaf	30.32—61.99	47.88	5.80	-0.39	0.84
	穗下叶Below the uppermost ear leaf	29.73—60.64	47.97	6.13	-0.33	0.52
2018年永城Yongcheng, 2018	穗上叶Above the uppermost ear leaf	40.92—69.59	54.67	6.61	0.00	0.00
	穗位叶Uppermost ear leaf	38.30—68.48	54.86	6.74	-0.20	0.37
	穗下叶Below the uppermost ear leaf	37.85—69.15	54.99	6.96	-0.03	-0.04
综合Blup	穗上叶Above the uppermost ear leaf	43.46—58.68	52.51	3.16	-0.57	1.02
	穗位叶Uppermost ear leaf	40.45—60.49	52.57	3.61	-0.55	0.78
	穗下叶Below the uppermost ear leaf	40.20—64.44	52.55	4.13	-0.50	0.64

性状 Trait	变异来源 Source	离均差平方和 Type sum of squares	自由度 Df	均方 Mean square	F值 F-value
穗上叶 Above the uppermost ear leaf	环境E	62052.294	4	15513.073	1202.047**
穗上叶 Above the uppermost ear leaf	基因型G	51835.582	537	96.528	7.479**
	基因型×环境 G×E	122215.029	2148	56.897	4.408**
	误差Error	138863.674	10760	12.906
	总变异Total	374966.579	13449
穗位叶 Uppermost ear leaf	环境E	74363.802	4	18590.951	1466.621**
穗位叶 Uppermost ear leaf	基因型G	56009.168	537	104.300	8.228**
	基因型×环境 G×E	126440.437	2148	58.864	4.643**
	误差Error	136394.238	10760	12.676
	总变异Total	393207.645	13449
穗下叶 Below the uppermost ear leaf	环境E	101559.963	4	25389.991	1822.287**
穗下叶 Below the uppermost ear leaf	基因型G	59378.695	537	110.575	7.936**
	基因型×环境 G×E	135210.636	2148	62.947	4.518**
	误差Error	149919.461	10760	13.933
	总变异Total	446068.755	13449

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Genome-Wide Association Study of Chlorophyll Content in Maize

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