玉米开花期转录因子候选基因的关联分析

doi:10.3864/j.issn.0578-1752.2022.01.002

中国农业科学 ›› 2022, Vol. 55 ›› Issue (1): 12-25.doi: 10.3864/j.issn.0578-1752.2022.01.002

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

玉米开花期转录因子候选基因的关联分析

马拴红¹(),万炯¹,梁瑞清²,张雪海¹,邱小倩¹,孟淑君¹,徐宁坤¹,林源¹,党昆泰¹,王琪月¹,赵嘉雯¹,丁冬¹(),汤继华¹()

¹河南农业大学农学院/省部共建小麦玉米作物学国家重点实验室,郑州 450002
²华南农业大学农学院,广州 510642

收稿日期:2021-07-07 接受日期:2021-09-03 出版日期:2022-01-01 发布日期:2022-01-07
通讯作者: 丁冬,汤继华
作者简介:马拴红,E-mail： 18838916904@163.com。
基金资助:
国家自然科学基金面上项目(31871641);国家自然科学基金面上项目(31971961);作物遗传与种质创新国家重点实验室开放课题(ZW202001);河南省科技攻关项目(202102110164);河南省科技攻关项目(202102110012)

Candidate Gene Association Analysis of Maize Transcription Factors in Flowering Time

MA ShuanHong¹(),WAN Jiong¹,LIANG RuiQing²,ZHANG XueHai¹,QIU XiaoQian¹,MENG ShuJun¹,XU NingKun¹,LIN Yuan¹,DANG KunTai¹,WANG QiYue¹,ZHAO JiaWen¹,DING Dong¹(),TANG JiHua¹()

¹College of Agronomy, Henan Agricultural University/National Key Laboratory of Wheat and Maize Crop Science, Zhengzhou 450002
²College of Agronomy, South China Agricultural University, Guangzhou 510642

Received:2021-07-07 Accepted:2021-09-03 Online:2022-01-01 Published:2022-01-07
Contact: Dong DING,JiHua TANG

摘要/Abstract

摘要：

【目的】生育期相关性状是玉米育种研究的重点之一。作为重要的生育期性状,开花期（抽穗期、吐丝期和散粉期）的提前,可保证玉米充分脱水,适宜机收;也为中国黄淮海地区小麦-玉米一年两熟耕作模式下的小麦播种减轻压力。转录因子是转录水平基因表达调控的重要上游因子,对目标基因发挥转录激活或转录抑制的作用。在全基因组水平上解析转录因子对玉米开花期的调控作用,获得开花期提前且不影响产量的玉米转录因子单倍型组合,进而挖掘优异种质资源,可为培育开花期适宜的玉米育种研究提供基因资源。【方法】使用候选基因关联分析方法,对开花期相关转录因子及显著SNP进行分析;并利用DAP-seq技术捕获了关键转录因子的结合位点和下游基因;随后对转录因子调控的下游基因进行GO分析,探究转录因子通过影响其下游基因对开花期进行调控的基因网络。【结果】玉米开花期3种性状（吐丝期、散粉期、抽穗期）中,与吐丝期和抽穗期性状以及吐丝期和散粉期性状同时关联的转录因子显著SNP均为75个,与抽穗期和散粉期性状同时关联的显著SNP为128个,同时关联到3种表型的显著SNP为58个。表明开花期3种性状可能受相同的转录因子调控。选取含有3个及以上开花期相关显著SNP的转录因子基因,通过DAP-seq,捕获了这些转录因子结合的关键基序及调控的下游基因。转录因子结合的下游基因显著富集于转录因子活性、DNA结合、RNA结合、有机氮化合物的合成代谢过程、与生殖有关的发育过程等;不同的转录因子存在共同调控的下游基因,生育期相关性状关键调控性转录因子为ARF、MYB和NAC。对关键上游转录因子进行单倍型分析,发掘了玉米生育期提前,同时对产量无负向影响的转录因子最优单倍型组合。【结论】运用DAP-seq技术并结合前人研究绘制了全基因组水平上转录因子对生育期相关农艺性状的调控网络,并发掘了既提前玉米生育期又对产量无负向影响的转录因子最优单倍型组合。

关键词: 玉米, 转录因子, 开花期, DAP-seq, 单倍型

Abstract:

【Objective】 Maize growth period traits, including flowering time, are the ones of most important in maize breeding. The advancement of heading date, silking time, and the pollen shed can ensure maize kernels fully dehydrated and thus suited to machinery harvesting. Moreover, the saved time can also leave for wheat sowing under the Maize-Wheat farming mode in Huang-Huai-Hai area. Transcription factors are important up-stream trans-action factors of gene expression regulation, which play roles in transcriptional activation or inhibition on target genes by binding to and driving their promoters. It is of great significance to analyze the regulatory effects of transcription factors on maize flowering time at the whole genome scale, it is also emergence to obtain the maize transcription factor haplotypes which associated with earlier flowering and higher yield. The haplotypes, or the haplotype combinations, will be served as excellent germplasm resources for maize breeding. 【Method】 In this study, candidate gene association analysis was performed to analyze maize flowering time related transcription factors and significant SNPs. DAP-seq was carried out to obtain the binding sites and down-stream genes of the key transcription factors. Followed by GO analysis on the down-stream genes to explore the transcription factor dependent gene expression regulatory network. 【Result】 There are 75, 75, and 128 significant SNPs detected in combinations of the traits Silking time and Heading date, the traits Silking time and Pollen shed, and the traits Heading date and Pollen shed, respectively. Altogether, there are 58 significant SNPs associated with all three flowering time traits. These results suggest that the three traits of flowering time may be regulated by the same transcription factors. Flowering time associated transcription factor genes that containing 3 or more significant SNPs were selected for DAP-seq to capture the key motifs and down-stream genes. Down-stream genes bound by flowering time associated transcription factors are significantly enriched in transcription factor activity, DNA binding, RNA binding, organonitrogen compound metabolic process, reproduction-related developmental processes, etc. Different transcription factors have co-regulated downstream genes related to flowering time. The key regulatory transcription factors for flowering time traits are ARF, MYB and NAC. Through haplotype analysis, the optimal TF haplotype combination that shows earlier flowering and no negative impact on yield was selected. 【Conclusion】 In this research, through candidate gene association and DAP-seq, the regulatory network of transcription factors on the flowering time related agronomic traits were established at the whole genome scale. The optimal haplotype combination of transcription factors that not only advances the flowering time, but also has no negative impact on yield was selected for further use in maize breeding.

Key words: maize, transcription factor, flowering time, DAP-seq, haplotype

马拴红, 万炯, 梁瑞清, 张雪海, 邱小倩, 孟淑君, 徐宁坤, 林源, 党昆泰, 王琪月, 赵嘉雯, 丁冬, 汤继华. 玉米开花期转录因子候选基因的关联分析[J]. 中国农业科学, 2022, 55(1): 12-25.

MA ShuanHong, WAN Jiong, LIANG RuiQing, ZHANG XueHai, QIU XiaoQian, MENG ShuJun, XU NingKun, LIN Yuan, DANG KunTai, WANG QiYue, ZHAO JiaWen, DING Dong, TANG JiHua. Candidate Gene Association Analysis of Maize Transcription Factors in Flowering Time[J]. Scientia Agricultura Sinica, 2022, 55(1): 12-25.

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图/表 9

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转录因子调控的下游基因"

基因 Gene ID	功能描述 Description	上游结合转录因子家族 Upstream binding TF families
Zm00001d017660	光周期非依赖性早花蛋白 1 Protein PHOTOPERIOD-INDEPENDENT EARLY FLOWERING 1	NAC/MYB/ARF/HB/C2C2-GATA/C2H2/WRKY/GRF/PLATZ
Zm00001d034036	多梳家族EMBRYONIC FLOWER 2蛋白 Polycomb group protein EMBRYONIC FLOWER 2	NAC/MYB/ARF
Zm00001d020364	早花蛋白4 Protein EARLY FLOWERING 4	NAC/MYB/ARF
Zm00001d047269	早花蛋白4 Protein EARLY FLOWERING 4	NAC/MYB/ARF
Zm00001d042066	糖苷水解酶家族2蛋白 Glycoside hydrolase family 2 protein	bZIP/HB/MYB/ARF
Zm00001d029378	LNK1蛋白Protein LNK1	AP2-EREBP/C2C2-GATA/C2H2/G2-like/MYB/NAC
Zm00001d035112	扩张蛋白A11 Expansin-A11	AP2-EREBP/C2C2-GATA/C2H2/G2-like/
Zm00001d037315	含NAC结构域的蛋白质8 NAC domain-containing protein 8	AP2-EREBP/C2C2-GATA/C2H2/G2-like/
Zm00001d048066	Sec14p样磷脂酰肌醇转移家族蛋白 Sec14p-like phosphatidylinositol transfer family protein	AP2-EREBP/C2C2-GATA/C2H2/G2-like/ARF/NAC
Zm00001d015082	转导家族蛋白/WD-40重复序列家族蛋白 Transducing family protein/WD-40 repeat family protein	WRKY/GRF/PLATZ/NLP/MYB/NAC
Zm00001d021147	蛋白酶体亚单位β-4型 Proteasome subunit beta type-4	WRKY/GRF/PLATZ/NLP/MYB/NAC/HB
Zm00001d034832	可能的叶绿体酰基激活酶16 Probable acyl-activating enzyme 16 chloroplastic	WRKY/GRF/PLATZ/NLP/MYB
Zm00001d037377	姐妹染色单体结合蛋白PDS5同源物A Sister chromatid cohesion protein PDS5 homolog A	WRKY/GRF/PLATZ/NLP/MYB/NAC
Zm00001d039518	真核起始因子3 Eukaryotic initiation factor3	WRKY/GRF/PLATZ/NLP/NAC/bZIP/HB/ARF
Zm00001d014895	推测的跨膜蛋白保守区（DUF2404） Putative integral membrane protein conserved region (DUF2404)	C2H2/G2-like/WRKY/GRFARF/NAC/MYB/HB
Zm00001d029329	多嘧啶结合束蛋白同源物1 Polypyrimidine tract-binding protein homolog 1	C2H2/G2-like/WRKY/GRFNAC/MYB
Zm00001d043093	MOR1蛋白 Protein MOR1	C2H2/G2-like/WRKY/GRFARF/NAC/MYB/HB
Zm00001d044566	胼胝质合酶7 Callose synthase 7	C2H2/G2-like/WRKY/GRFNAC/MYB

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表型 Trait	SNP数量 Number	转录因子家族 TF families
抽穗期 Heading date	206	AP2-EREBP、ARF、ARID、AUX/IAA、bHLH、bZIP、C2C2-DOF、C2C2-GATA、C2C2-YABBY、C3H、CCAAT-HAP2、coactivator-p15、DDT、G2-like、GNAT、GRAS、GRF、HB、HSF、LOB、MADS、MYB、MYB-related、NAC、NLP、OFP、Orphans、PHD、PLATZ、Rcd1-like、TCP、TRAF、Trihelix、WRKY
吐丝期 Silking time	168	ABI3VP1、AP2-EREBP、ARF、AUX/IAA、bHLH、bZIP、C2C2-GATA、C2H2、C3H、coactivator-p15、DDT、G2-like、GRAS、GRF、HB、IWS1、MADS、mTERF、MYB、MYB-related、NAC、NLP、Orphans、PHD、Rcd1-like、SNF2、TAZ、WRKY
散粉期 Pollen shed	177	AP2-EREBP、ARF、AUX/IAA、bHLH、bZIP、C2C2-DOF、C2C2-GATA、C2H2、C3H、CCAAT-HAP2、DDT、G2-like、GNAT、GRAS、HB、IWS1、MADS、MYB、MYB-related、NAC、NLP、Orphans、PHD、Rcd1-like、Trihelix、WRKY
抽穗/吐丝 Heading date/Silking time	75	AP2-EREBP、ARF、AUX/IAA、bHLH、bZIP、C2C2-GATA、coactivator-p15、DDT、G2-like、MADS、MYB、NAC、NLP、Orphans、PHD、Rcd1-like、WRKY
抽穗/散粉 Heading date/Pollen shed	125	AP2-EREBP、ARF、bHLH、bZIP、C2C2-DOF、C2C2-GATA、C3H、CCAAT-HAP2、DDT、G2-like、GNAT、HB、MYB、MYB-related、NAC、NLP、Orphans、PHD、Rcd1-like、Trihelix、WRKY
吐丝/散粉 Silking time/Pollen shed	75	AP2-EREBP、ARF、bHLH、bZIP、C2C2-GATA、C2H2、DDT、G2-like、GRAS、IWS1、MYB、NAC、NLP、Orphans、PHD、Rcd1-like、WRKY
抽穗/吐丝/散粉 Heading date/Silking time/Pollen shed	58	AP2-EREBP、ARF、bHLH、bZIP、C2C2-GATA、DDT、G2-like、MYB、NAC、NLP、Orphans、PHD、Rcd1-like、WRKY

单倍型组合 Haplotype combination	表型值 Phenotypic value		份数 Number	表型值 Phenotypic value		份数 Number	表型值 Phenotypic value		份数 Number
单倍型组合 Haplotype combination	单穗产量 Yield per ear	抽穗期 Heading date	份数 Number	单穗产量 Yield per ear	吐丝期 Silking time	份数 Number	单穗产量 Yield per ear	散粉期 Pollen shed	份数 Number
A1	41.66	62.29	28	40.27	67.40	22	41.66	65.30	28
B1	41.45	63.97	27	-	69.11	-	41.45	66.79	27
C1	42.76	63.35	27	44.29	68.58	10	42.43	66.29	27
A2	45.21	67.55	424	45.21	72.43	414	45.14	70.41	424
B2	45.22	67.48	425	-	72.34	-	45.22	70.34	425
C2	45.17	67.54	424	45.16	72.38	424	45.20	70.39	424
A2B2	45.30	67.64	410	-	-	-	45.23	70.51	409
A2C2	45.30	67.73	402	45.29	72.47	414	45.23	70.58	401
B2C2	45.37	67.74	398	-	-	-	45.37	70.59	398
A2B2C2	45.12	67.81	389	-	-	-	45.30	70.67	388
A1B1	40.20	62.77	13	-	-	-	40.20	65.56	13
A1C1	39.89	61.92	9	41.85	66.49	4	40.44	64.22	9
A1B2	42.93	63.29	15	-	-	-	44.30	67.05	11
A1C2	42.50	63.58	19	39.28	67.24	15	43.74	67.05	14
A2B1	42.61	65.09	14	-	-	-	42.61	67.93	14
A2C1	44.28	64.06	18	45.69	69.70	5	44.23	67.12	17
B1C1	39.88	63.38	4				38.68	65.65	5
B1C2	41.72	64.07	23				42.08	67.05	22
B2C1	43.28	63.34	23				43.28	66.25	23
A1B1C1	40.20	63.76	3	-	-	-	38.62	65.24	4
A1B2C1	39.73	60.99	6	-	-	-	39.73	63.53	6
A1B2C2	45.06	64.82	9	-	-	-	45.06	67.79	9
A1B1C2	40.20	62.47	10	-	-	-	40.90	65.71	9
A2B1C2	-	-	-	-	-	-	42.90	67.98	13
A2B2C1	-	-	-	-	-	-	44.61	67.20	17

玉米开花期转录因子候选基因的关联分析

Candidate Gene Association Analysis of Maize Transcription Factors in Flowering Time

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