Geneome-Wide Identification and Expression Analysis of Auxin Response Factor Gene Family in Maize

doi:10.11869/j.issn.100-8551.2021.09.2016

Journal of Nuclear Agricultural Sciences ›› 2021, Vol. 35 ›› Issue (9): 2016-2026.DOI: 10.11869/j.issn.100-8551.2021.09.2016

• Induced Mutations for Plant Breeding·Agricultural Biotechnology • Previous Articles Next Articles

Geneome-Wide Identification and Expression Analysis of Auxin Response Factor Gene Family in Maize

CAO Liru¹(), ZHANG Qianjin¹, GUO Zining², LU Xiaomin¹, ZHANG Xin¹, WEI Xin¹, HUANG-FU Baishu³^,^*(), WANG Zhenhua¹^,^*()

¹ Grain Crop Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou, Henan 450002
² Science and Technology Achievement Demonstration and Promotion Division, Henan Academy of Agricultural Sciences, Zhengzhou, Henan 450002
³ Jiaozuo Academy of Agriculture and Forestry Sciences, Jiaozuo, Henan 454150

Received:2020-06-28 Accepted:2020-10-04 Online:2021-09-10 Published:2021-07-22
Contact: HUANG-FU Baishu,WANG Zhenhua

玉米生长素响应因子基因家族全基因组鉴定及表达分析

曹丽茹¹(), 张前进¹, 郭子宁², 鲁晓民¹, 张新¹, 魏昕¹, 皇甫柏树³^,^*(), 王振华¹^,^*()

¹ 河南省农业科学院粮食作物研究所,河南郑州 450002
² 河南省农业科学院科技成果示范推广处, 河南郑州 450002
³ 焦作市农林科学研究院,河南焦作 454150

通讯作者: 皇甫柏树,王振华
作者简介:曹丽茹,女,主要从事玉米遗传育种及生物信息学分析。E-mail: caoliru008@126.com
基金资助:
河南省农业科学院杰出青年发展基金(2020JQ02)

Abstract

Abstract:

Auxin response factor (ARF) can specifically bind to the promoter region of response gene to regulate plant growth and development. In order to understand furtherly the number, basic characteristics, evolutionary relationship of ARF gene family in maize and the expression pattern of ARF in response to abiotic stress and hormone. In this study, the ARF gene family in maize was identified by bioinformatics, and the physiochemical properties and the phylogeny of proteins were analyzed. RT-qPCR was used to analyze the temporal and spatial expression patterns and their expression under high temperature, drought, salt and ABA treatment of fourZmARFs. The results showed that 36 ARFs genes were randomly and unevenly distributed on 9 chromosomes, and the amino acid length, molecular weight, isoelectric point and secondary structure of the encoding protein were quite different. The protein phylogenetic tree of sorghum, rice, Arabidopsis and maize showed that these ARF proteins are divided into four categories Ⅰ~Ⅳ. Maize ARF has the closest genetic relationship with sorghum ARF, and the farthest genetic relationship with Arabidopsis ARF, and there were intragenic and intergenic duplication occurs in maize.The cis-acting elements of promoter are main elements in response to drought, low temperature, oxidation and hormones. RT-qPCR results showed that the expression of ZmARF1,ZmARF6,ZmARF13 and ZmARF22 were higher in the tassel branches and embryos, but lower in the pollen. The four genes were significantly up-regulated when induced by high temperature, drought, salt and ABA, except that ZmARF22 gene had decreased expression after high temperature treatment. Subcellular localization indicated that the proteins encoded byZmARF1, ZmARF6, ZmARF13 and ZmARF22 are localized in the nucleus. The results of this study provide a theoretical basis for revealing the function of maize ARF protein and mining stress resistant genes, and also provide molecular resources for stress resistant breeding.

Key words: maize, ZmARFs, bioinformatics, expression pattern, cell nucleus

摘要：

生长素响应因子(ARF)在植物中可以特异性结合在应答基因的启动子区域,调控植物的生长发育。为了进一步了解玉米ARF基因家族的数量、基本特征、进化关系及响应非生物胁迫和激素的表达模式,本研究在全基因组水平,通过生物信息学方法鉴定玉米ARF基因家族,分析了蛋白理化性质及系统发育,利用实时荧光定量PCR(RT-qPCR)分析了4个ZmARFs基因的时空表达模式及高温、干旱、盐和脱落酸(ABA)处理下的表达情况。结果表明,玉米36个ARFs基因随机非均匀分布在9条染色体上,编码氨基酸长度、分子量、等电点及二级结构存在很大的差异。高粱、水稻、拟南芥和玉米的蛋白复合进化树显示共分为Ⅰ~Ⅳ四大类,玉米与高粱ARF蛋白亲缘关系最近,而与拟南芥ARF蛋白亲缘关系最远,且玉米中发生基因内和基因间复制现象。启动子顺式作用元件主要是干旱、低温、氧化和激素类响应元件。RT-qPCR结果显示,ZmARF1、ZmARF6、ZmARF13和ZmARF22基因均在雄穗分支和胚中表达量较高,在花粉中表达量较低;4个基因(除ZmARF22)在高温、干旱、盐和ABA诱导时均显著上调表达。亚细胞定位表明上述4个基因编码的蛋白质均定位于细胞核。本研究结果为揭示玉米ARF蛋白功能和挖掘玉米的抗逆基因提供了理论基础,为抗逆育种提供了分子资源。

关键词: 玉米, ZmARFs, 生物信息学, 表达模式, 细胞核

CAO Liru, ZHANG Qianjin, GUO Zining, LU Xiaomin, ZHANG Xin, WEI Xin, HUANG-FU Baishu, WANG Zhenhua. Geneome-Wide Identification and Expression Analysis of Auxin Response Factor Gene Family in Maize[J]. Journal of Nuclear Agricultural Sciences, 2021, 35(9): 2016-2026.

曹丽茹, 张前进, 郭子宁, 鲁晓民, 张新, 魏昕, 皇甫柏树, 王振华. 玉米生长素响应因子基因家族全基因组鉴定及表达分析[J]. 核农学报, 2021, 35(9): 2016-2026.

Figures/Tables 9

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创刊：1987年
主管部门：农业农村部
主办单位：中国原子能农学会与中国农业科学院农产品加工研究所（前中国农业科学院原子能利用研究所）
ISSN：1000-8551

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基因编号 Gene name	基因ID Gene ID	长度 Length/aa	结构域 Domain	分子量 Molecular weight/kDa	等电点 pI	ɑ-螺旋 ɑ-Helix /%	β-转角 β-Turn /%	无规则卷曲 Random coil/%	延伸链 Extender china/%
ZmARF1	Zm00001d031064	897	B3,ARF,AUX_IAA	98.37	6.23	29.21	8.47	45.82	16.50
ZmARF2	Zm00001d032683	681	B3,ARF	74.54	7.92	18.21	4.41	61.53	15.86
ZmARF3	Zm00001d031522	1 086	B3,ARF,AUX_IAA	120.17	6.25	27.99	6.91	45.40	19.71
ZmARF4	Zm00001d030801	446	B3,ARF	48.73	8.66	14.35	3.81	59.64	22.20
ZmARF5	Zm00001d030803	418	B3,ARF	46.83	7.07	18.66	3.59	57.89	19.86
ZmARF6	Zm00001d003601	657	B3,ARF,AUX_IAA	72.95	6.14	25.27	4.26	54.64	15.83
ZmARF7	Zm00001d001945	935	B4,ARF,AUX_IAA	102.87	6.12	26.95	7.17	50.37	15.51
ZmARF8	Zm00001d001879	817	B5,ARF,AUX_IAA	90.99	6.37	30.11	6.24	47.12	16.52
ZmARF9	Zm00001d003011	273	B3,ARF	29.73	7.58	17.95	5.86	56.78	19.41
ZmARF10	Zm00001d002929	513	B3,ARF	55.45	6.40	14.81	3.51	65.50	16.18
ZmARF11	Zm00001d043431	688	B3,ARF	74.99	7.28	16.42	4.94	64.97	13.66
ZmARF12	Zm00001d041497	888	B5,ARF,AUX_IAA	97.84	6.08	29.73	8.00	46.96	15.32
ZmARF13	Zm00001d042267	822	B6,ARF,AUX_IAA	91.85	6.91	19.83	4.99	59.73	15.45
ZmARF14	Zm00001d041056	652	B7,ARF,AUX_IAA	71.86	7.43	15.95	3.53	65.18	15.34
ZmARF15	Zm00001d043922	708	B3,ARF	77.97	7.11	14.69	4.24	66.10	14.97
ZmARF16	Zm00001d039267	686	B3,ARF	76.72	6.29	19.97	4.52	57.58	17.93
ZmARF17	Zm00001d053819	914	B7,ARF,AUX_IAA	100.94	6.03	29.65	4.92	52.08	13.35
ZmARF18	Zm00001d051172	689	B3,ARF	73.69	7.36	20.39	4.78	61.04	13.78
ZmARF19	Zm00001d050781	511	B7,ARF,AUX_IAA	56.73	6.83	19.77	4.89	55.38	19.96
ZmARF20	Zm00001d049295	850	B7,ARF,AUX_IAA	93.15	7.01	20.82	5.41	58.47	15.29
ZmARF21	Zm00001d014507	716	B3,ARF	77.52	7.13	19.17	4.41	60.28	16.14
ZmARF22	Zm00001d014377	739	B7,ARF,AUX_IAA	82.00	6.99	24.63	5.01	54.80	15.56
ZmARF23	Zm00001d015243	1 147	B7,ARF,AUX_IAA	127.24	6.08	33.48	6.54	42.55	17.44
ZmARF24	Zm00001d014013	644	B3,ARF	70.96	6.97	19.57	4.66	59.94	15.84
ZmARF25	Zm00001d014690	975	B7,ARF,AUX_IAA	107.54	6.60	30.87	7.08	47.38	14.67
ZmARF26	Zm00001d016838	677	B7,ARF,AUX_IAA	75.13	6.30	19.50	4.58	59.23	16.69
ZmARF27	Zm00001d039006	736	B3,ARF	80.42	7.83	15.22	4.08	65.08	15.62
ZmARF28	Zm00001d000358	700	B3,ARF	75.51	7.56	17.86	4.29	61.14	16.71
ZmARF29	Zm00001d038698	680	B3,ARF	73.94	6.86	16.18	4.41	66.32	13.09
ZmARF30	Zm00001d011953	728	B7,ARF,AUX_IAA	81.43	7.66	15.25	3.16	65.66	15.93
ZmARF31	Zm00001d012731	340	B3,ARF	37.38	7.95	23.24	5.00	49.41	22.35
ZmARF32	Zm00001d025871	588	B3,ARF	63.91	8.77	18.54	4.08	63.10	14.29
ZmARF33	Zm00001d023659	813	B7,ARF,AUX_IAA	89.71	7.25	20.33	4.09	59.75	15.83
ZmARF34	Zm00001d026687	462	B3,ARF	50.56	5.41	17.32	3.68	58.01	21.00
ZmARF35	Zm00001d026540	958	B7,ARF,AUX_IAA	105.29	6.44	28.50	4.91	53.03	13.57
ZmARF36	Zm00001d045026	1 053	B7,ARF,AUX_IAA	116.75	6.67	37.42	6.84	42.36	13.39

基因编号 Gene name	基因ID Gene ID	长度 Length/aa	结构域 Domain	分子量 Molecular weight/kDa	等电点 pI	ɑ-螺旋 ɑ-Helix /%	β-转角 β-Turn /%	无规则卷曲 Random coil/%	延伸链 Extender china/%
ZmARF1	Zm00001d031064	897	B3,ARF,AUX_IAA	98.37	6.23	29.21	8.47	45.82	16.50
ZmARF2	Zm00001d032683	681	B3,ARF	74.54	7.92	18.21	4.41	61.53	15.86
ZmARF3	Zm00001d031522	1 086	B3,ARF,AUX_IAA	120.17	6.25	27.99	6.91	45.40	19.71
ZmARF4	Zm00001d030801	446	B3,ARF	48.73	8.66	14.35	3.81	59.64	22.20
ZmARF5	Zm00001d030803	418	B3,ARF	46.83	7.07	18.66	3.59	57.89	19.86
ZmARF6	Zm00001d003601	657	B3,ARF,AUX_IAA	72.95	6.14	25.27	4.26	54.64	15.83
ZmARF7	Zm00001d001945	935	B4,ARF,AUX_IAA	102.87	6.12	26.95	7.17	50.37	15.51
ZmARF8	Zm00001d001879	817	B5,ARF,AUX_IAA	90.99	6.37	30.11	6.24	47.12	16.52
ZmARF9	Zm00001d003011	273	B3,ARF	29.73	7.58	17.95	5.86	56.78	19.41
ZmARF10	Zm00001d002929	513	B3,ARF	55.45	6.40	14.81	3.51	65.50	16.18
ZmARF11	Zm00001d043431	688	B3,ARF	74.99	7.28	16.42	4.94	64.97	13.66
ZmARF12	Zm00001d041497	888	B5,ARF,AUX_IAA	97.84	6.08	29.73	8.00	46.96	15.32
ZmARF13	Zm00001d042267	822	B6,ARF,AUX_IAA	91.85	6.91	19.83	4.99	59.73	15.45
ZmARF14	Zm00001d041056	652	B7,ARF,AUX_IAA	71.86	7.43	15.95	3.53	65.18	15.34
ZmARF15	Zm00001d043922	708	B3,ARF	77.97	7.11	14.69	4.24	66.10	14.97
ZmARF16	Zm00001d039267	686	B3,ARF	76.72	6.29	19.97	4.52	57.58	17.93
ZmARF17	Zm00001d053819	914	B7,ARF,AUX_IAA	100.94	6.03	29.65	4.92	52.08	13.35
ZmARF18	Zm00001d051172	689	B3,ARF	73.69	7.36	20.39	4.78	61.04	13.78
ZmARF19	Zm00001d050781	511	B7,ARF,AUX_IAA	56.73	6.83	19.77	4.89	55.38	19.96
ZmARF20	Zm00001d049295	850	B7,ARF,AUX_IAA	93.15	7.01	20.82	5.41	58.47	15.29
ZmARF21	Zm00001d014507	716	B3,ARF	77.52	7.13	19.17	4.41	60.28	16.14
ZmARF22	Zm00001d014377	739	B7,ARF,AUX_IAA	82.00	6.99	24.63	5.01	54.80	15.56
ZmARF23	Zm00001d015243	1 147	B7,ARF,AUX_IAA	127.24	6.08	33.48	6.54	42.55	17.44
ZmARF24	Zm00001d014013	644	B3,ARF	70.96	6.97	19.57	4.66	59.94	15.84
ZmARF25	Zm00001d014690	975	B7,ARF,AUX_IAA	107.54	6.60	30.87	7.08	47.38	14.67
ZmARF26	Zm00001d016838	677	B7,ARF,AUX_IAA	75.13	6.30	19.50	4.58	59.23	16.69
ZmARF27	Zm00001d039006	736	B3,ARF	80.42	7.83	15.22	4.08	65.08	15.62
ZmARF28	Zm00001d000358	700	B3,ARF	75.51	7.56	17.86	4.29	61.14	16.71
ZmARF29	Zm00001d038698	680	B3,ARF	73.94	6.86	16.18	4.41	66.32	13.09
ZmARF30	Zm00001d011953	728	B7,ARF,AUX_IAA	81.43	7.66	15.25	3.16	65.66	15.93
ZmARF31	Zm00001d012731	340	B3,ARF	37.38	7.95	23.24	5.00	49.41	22.35
ZmARF32	Zm00001d025871	588	B3,ARF	63.91	8.77	18.54	4.08	63.10	14.29
ZmARF33	Zm00001d023659	813	B7,ARF,AUX_IAA	89.71	7.25	20.33	4.09	59.75	15.83
ZmARF34	Zm00001d026687	462	B3,ARF	50.56	5.41	17.32	3.68	58.01	21.00
ZmARF35	Zm00001d026540	958	B7,ARF,AUX_IAA	105.29	6.44	28.50	4.91	53.03	13.57
ZmARF36	Zm00001d045026	1 053	B7,ARF,AUX_IAA	116.75	6.67	37.42	6.84	42.36	13.39

顺式元件 Cis-element	序列 Sequence	功能 Function	基因 Gene
ABRE	ACGTG	脱落酸响应元件	ZmARF1,ZmARF3~ZmARF17,ZmARF20~ZmARF26, ZmARF27~ZmARF36
ARE	AAACCA	与厌氧诱导相关的调控元件	ZmARF4,ZmARF5,ZmARF8,ZmARF9,ZmARF12~ZmARF21, ZmARF23,ZmARF25,ZmARF26,ZmARF29,ZmARF32, ZmARF33,ZmARF35
AuxRR-core	GGTCCAT	调控生长素响应元件	ZmARF1,ZmARF2,ZmARF7,ZmARF14,ZmARF17~ZmARF20, ZmARF22,ZmARF25,ZmARF26,ZmARF28,ZmARF35
CAT-box	GCCACT	分生组织表达相关的元件	ZmARF1~ZmARF3
TGACG-motif/ CGTCA-motif	TGACG/CGTCA	茉莉酸甲酯响应元件	ZmARF1~ZmARF13,ZmARF15~ZmARF26, ZmARF28-ZmARF32,ZmARF35,ZmARF36
GARE-motif	TCTGTTG	赤霉素反应元件	ZmARF2,ZmARF3,ZmARF8,ZmARF17,ZmARF26, ZmARF30,ZmARF31,ZmARF34-ZmARF36
GCN4-motif	TGAGTCA	胚乳表达相关的元件	ZmARF1,ZmARF4,ZmARF6,ZmARF14, ZmARF18~ZmARF20,ZmARF29,ZmARF32
LTR	CCGAAA	低温响应	ZmARF1~ZmARF3,ZmARF8,ZmARF11~ZmARF13, ZmARF18~ZmARF22,ZmARF24~ZmARF26,ZmARF28, ZmARF29,ZmARF33
MBS	CAACTG	干旱诱导的MYB结合位点	ZmARF1,ZmARF3~ZmARF7,ZmARF10~ZmARF13, ZmARF15~ZmARF20,ZmARF25,ZmARF26,ZmARF28, ZmARF30,ZmARF31,ZmARF34,ZmARF35
TCA-element	CCATCTTTTT	水杨酸反应元件	ZmARF1~ZmARF3,ZmARF5,ZmARF8,ZmARF10~ZmARF12, ZmARF14,ZmARF17,ZmARF20,ZmARF21,ZmARF24 ~ZmARF26,ZmARF28,ZmARF29,ZmARF32,ZmARF34
TC-rich repeats	ATTCTCTAAC	参与防御和应激反应	ZmARF1,ZmARF5,ZmARF7,ZmARF13,,ZmARF16, ZmARF17,ZmARF19,ZmARF29,ZmARF35
TGA-element	AACGAC	生长素反应元件	ZmARF2,ZmARF8,ZmARF16~ZmARF18,ZmARF20 ~ZmARF22,ZmARF24,ZmARF28,ZmARF30, ZmARF35

顺式元件 Cis-element	序列 Sequence	功能 Function	基因 Gene
ABRE	ACGTG	脱落酸响应元件	ZmARF1,ZmARF3~ZmARF17,ZmARF20~ZmARF26, ZmARF27~ZmARF36
ARE	AAACCA	与厌氧诱导相关的调控元件	ZmARF4,ZmARF5,ZmARF8,ZmARF9,ZmARF12~ZmARF21, ZmARF23,ZmARF25,ZmARF26,ZmARF29,ZmARF32, ZmARF33,ZmARF35
AuxRR-core	GGTCCAT	调控生长素响应元件	ZmARF1,ZmARF2,ZmARF7,ZmARF14,ZmARF17~ZmARF20, ZmARF22,ZmARF25,ZmARF26,ZmARF28,ZmARF35
CAT-box	GCCACT	分生组织表达相关的元件	ZmARF1~ZmARF3
TGACG-motif/ CGTCA-motif	TGACG/CGTCA	茉莉酸甲酯响应元件	ZmARF1~ZmARF13,ZmARF15~ZmARF26, ZmARF28-ZmARF32,ZmARF35,ZmARF36
GARE-motif	TCTGTTG	赤霉素反应元件	ZmARF2,ZmARF3,ZmARF8,ZmARF17,ZmARF26, ZmARF30,ZmARF31,ZmARF34-ZmARF36
GCN4-motif	TGAGTCA	胚乳表达相关的元件	ZmARF1,ZmARF4,ZmARF6,ZmARF14, ZmARF18~ZmARF20,ZmARF29,ZmARF32
LTR	CCGAAA	低温响应	ZmARF1~ZmARF3,ZmARF8,ZmARF11~ZmARF13, ZmARF18~ZmARF22,ZmARF24~ZmARF26,ZmARF28, ZmARF29,ZmARF33
MBS	CAACTG	干旱诱导的MYB结合位点	ZmARF1,ZmARF3~ZmARF7,ZmARF10~ZmARF13, ZmARF15~ZmARF20,ZmARF25,ZmARF26,ZmARF28, ZmARF30,ZmARF31,ZmARF34,ZmARF35
TCA-element	CCATCTTTTT	水杨酸反应元件	ZmARF1~ZmARF3,ZmARF5,ZmARF8,ZmARF10~ZmARF12, ZmARF14,ZmARF17,ZmARF20,ZmARF21,ZmARF24 ~ZmARF26,ZmARF28,ZmARF29,ZmARF32,ZmARF34
TC-rich repeats	ATTCTCTAAC	参与防御和应激反应	ZmARF1,ZmARF5,ZmARF7,ZmARF13,,ZmARF16, ZmARF17,ZmARF19,ZmARF29,ZmARF35
TGA-element	AACGAC	生长素反应元件	ZmARF2,ZmARF8,ZmARF16~ZmARF18,ZmARF20 ~ZmARF22,ZmARF24,ZmARF28,ZmARF30, ZmARF35

Geneome-Wide Identification and Expression Analysis of Auxin Response Factor Gene Family in Maize

玉米生长素响应因子基因家族全基因组鉴定及表达分析

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