高粱TGA基因响应孢堆黑粉菌（Sporisorium reilianum）侵染表达和DNA变异分析

doi:10.13560/j.cnki.biotech.bull.1985.2024-0979

生物技术通报 ›› 2025, Vol. 41 ›› Issue (5): 90-103.doi: 10.13560/j.cnki.biotech.bull.1985.2024-0979

高粱TGA基因响应孢堆黑粉菌（Sporisorium reilianum）侵染表达和DNA变异分析

刘卓君¹(), 柴文婷¹, 任毅乐¹, 王新宇¹, 朱立勋¹, 赵珊珊¹, 杨博慧¹, 范佳利¹, 李新凤¹, 赵威军², 吕晋慧³, 张春来¹^,⁴()

^1.山西农业大学农学院山西省/教育部共建作物高产优质协同创新中心，太谷 030801
^2.山西农业大学高粱研究所，榆次 030600
^3.山西农业大学林学院，太谷 030801
^4.后稷山西省实验室，太原 030031

收稿日期:2024-10-08 出版日期:2025-05-26 发布日期:2025-06-05
通讯作者: 张春来，男，博士，教授，研究方向：作物基因组与分子育种；E-mail: chunlaiz@hotmail.com
作者简介:刘卓君，女，硕士研究生，研究方向：作物基因组与分子育种；E-mail: 13834084336@163.com
第一联系人：（刘卓君、柴文婷并列第一作者）
基金资助:
基金项目:国家自然科学基金项目(31971994);山西省教育厅研究生实践创新(2023SJ109);山西农科院博士基金项目(ybsjj1404);山西省教育厅重点专业建设项目(J20220211)

Analysis on Expression and DNA Variation of TGA Genes in Sorghum （Sorghum bicolor） in Response to Sporisorium reilianum Infection

LIU Zhuo-jun¹(), CHAI Wen-ting¹, REN Yi-le¹, WANG Xin-yu¹, ZHU Li-xun¹, ZHAO Shan-shan¹, YANG Bo-hui¹, FAN Jia-li¹, LI Xin-feng¹, ZHAO Wei-jun², LYU Jin-hui³, ZHANG Chun-lai¹^,⁴()

^1.College of Agronomy, Shanxi Province/Ministry of Education Collaborative Innovation Center for High Yield and High Quality Crops, Shanxi Agricultural University, Taigu 030801
^2.Institute of Sorghum, Shanxi Agricultural University, Yuci 030600
^3.College of Forestry, Shanxi Agricultural University, Taigu 030801
^4.Houji Shanxi Province Laboratory, Taiyuan 030031

Received:2024-10-08 Published:2025-05-26 Online:2025-06-05

摘要/Abstract

摘要：

目的 TGA基因亚家族是bZIP转录因子家族中十分重要的成员。鉴定高粱基因组TGA基因家族成员，进行基因表达和自然等位变异分析，筛选出响应孢堆黑粉菌侵染的TGA基因和顺式作用元件。方法在高粱全基因组鉴定SbTGAs基因家族成员，并进行染色体定位、基因结构、蛋白理化性质、进化关系、顺式作用元件和共线性分析，分析在丝黑穗病菌侵染下SbTGAs的转录表达特性，检测在高粱种质自然群体的DNA变异。结果高粱基因组中共有17个SbTGAs家族成员，均含有DOG1结构域，多数有bZIP结构域，定位于细胞核，大部分的SbTGA基因内含子数量为3‒12，聚类分析表明，高粱TGA基因家族基因可分为5个亚族。玉米与高粱15个TGA基因存在共线性，亲缘关系更近。基因表达分析表明，SbTGA2.1b在高粱的根和叶中显著表达，丝黑穗病菌侵染后，SbTGA2.1b的表达在抗、感丝黑穗病品系显著诱导； SbTGA2.2、SbTGA5和SbTGA6.6g的表达在感病株受抑制；在高粱种质检测到SbTGA2.1a和SbTGA6.6g等5个基因多个非同义SNP变异和插入缺失（INDEL）变异。结论 SbTGA2.1b等响应孢堆黑粉菌侵染，存在非同义SNP变异和INDEL变异高粱种质，为高粱抗丝黑穗病的分子育种提供依据。

关键词: 高粱, TGA, 孢堆黑粉菌, 基因表达, DNA变异

Abstract:

Objective The TGA family is a very important group of bZIP transcription factors. This study is aimed to identify the TGA gene family members of the sorghum genome, analyse gene expression and natural allele variation analysis, and screen the genes and cis-acting elements that respond to the infection of Sporisorium reilianum. Method We identified the members of SbTGAs gene family in the whole genome through bioinformatic and molecular biological methods, and analysed their chromosome location, gene structure, protein physicochemical properties, evolutionary relationship, cis-regulatory elements of their putative promoters, collinearity analysis, and transcriptional expression characteristics after the infection of head smut fungus. Result In sorghum genome there were 17 SbTGA family members, all of them contained the DOG1 domain and most carried bZIP domain. All SbTGAs were located in the nucleus, and most of the SbTGA gene had 3‒12 introns. Phylogenetic analysis showed that the TGA gene family could be divided into five subfamilies. There were 15 genes in Zea mays having collinearity withsorghum, and their genetic relationships were closer. Gene expression analysis showed that the expressions of SbTGA2.1b were significant in the roots and leaves, and significantly induced after infection by S. reilianum in both lines with resistance and susceptability to head smut. It can be seen that the expressions of SbTGA2.2, SbTGA5 and SbTGA6.6g in healthy lines were up-regulated compared with that in susceptible lines. The synthetic analysis of whole genome resequencing data revealed five genes, including SbTGA2.1a and SbTGA6.6g, carrying multiple non-synonymous SNP and INDEL variations. Conclusion SbTGAs including SbTGA2.1b are hypothesized to associate with sorghum head smut resistance. These findings provide an evidences for breeding sorghum for resistance to head smut.

Key words: sorghum, TGA, head smut fungus Sporisorium reilianum, gene expression, DNA variation

刘卓君, 柴文婷, 任毅乐, 王新宇, 朱立勋, 赵珊珊, 杨博慧, 范佳利, 李新凤, 赵威军, 吕晋慧, 张春来. 高粱TGA基因响应孢堆黑粉菌（Sporisorium reilianum）侵染表达和DNA变异分析[J]. 生物技术通报, 2025, 41(5): 90-103.

LIU Zhuo-jun, CHAI Wen-ting, REN Yi-le, WANG Xin-yu, ZHU Li-xun, ZHAO Shan-shan, YANG Bo-hui, FAN Jia-li, LI Xin-feng, ZHAO Wei-jun, LYU Jin-hui, ZHANG Chun-lai. Analysis on Expression and DNA Variation of TGA Genes in Sorghum （Sorghum bicolor） in Response to Sporisorium reilianum Infection[J]. Biotechnology Bulletin, 2025, 41(5): 90-103.

图/表 17

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基因编号 Gene ID	基因名称 Gene name	染色体 Chromosome	基因位置 Genome location （bp）	基因长度 Length （bp）
Sobic.003G329500	SbTGA1.3g	03	65 465 408‒65 471 285	5 877
Sobic.009G180700 Sobic.002G247300 Sobic.002G424000	SbTGA1.9g SbTGA2.1a SbTGA2.1b	09 02 02	53 491 550‒53 494 415 63 528 681‒63 539 526 77 105 916‒77 111 030	3 266 10 846 5 114
Sobic.001G390800	SbTGA2.2	01	67 724 716‒67 732 814	8 098
Sobic.003G081000	SbTGA2.3	03	6 962 855‒6 973 141	10 286
Sobic.010G110100	SbTGA3	10	11 004 657‒11 007 712	3 055
Sobic.005G038700	SbTGA4.5g	05	3 538 193‒3 544 684	6 491
Sobic.008G037900 Sobic.003G363600 Sobic.009G155050	SbTGA4.8g SbLG2 SbTGA5	08 03 09	3 557 720‒3 568 195 68 107 428‒68 115 976 51 158 262‒51 167 491	10 476 8 549 9 128
Sobic.006G233500	SbTGA6.6g	06	57 541 249‒57 549 389	8 140
Sobic.007G061100 Sobic.002G153100	SbTGA6.7g SbTGA7	07 02	6 413 340‒ 6 427 344 45 762 133‒45 770 211	14 005 8 078
Sobic.010G192366	SbTGA8	10	53 452 812‒53 453 964	1 152
Sobic.004G078800	SbTGA9	04	6 496 341‒6 505 629	9 288
Sobic.001G243800	SbTGA10	01	25 331 187‒25 332 625	1 438

基因编号 Gene ID	基因名称 Gene name	染色体 Chromosome	基因位置 Genome location （bp）	基因长度 Length （bp）
Sobic.003G329500	SbTGA1.3g	03	65 465 408‒65 471 285	5 877
Sobic.009G180700 Sobic.002G247300 Sobic.002G424000	SbTGA1.9g SbTGA2.1a SbTGA2.1b	09 02 02	53 491 550‒53 494 415 63 528 681‒63 539 526 77 105 916‒77 111 030	3 266 10 846 5 114
Sobic.001G390800	SbTGA2.2	01	67 724 716‒67 732 814	8 098
Sobic.003G081000	SbTGA2.3	03	6 962 855‒6 973 141	10 286
Sobic.010G110100	SbTGA3	10	11 004 657‒11 007 712	3 055
Sobic.005G038700	SbTGA4.5g	05	3 538 193‒3 544 684	6 491
Sobic.008G037900 Sobic.003G363600 Sobic.009G155050	SbTGA4.8g SbLG2 SbTGA5	08 03 09	3 557 720‒3 568 195 68 107 428‒68 115 976 51 158 262‒51 167 491	10 476 8 549 9 128
Sobic.006G233500	SbTGA6.6g	06	57 541 249‒57 549 389	8 140
Sobic.007G061100 Sobic.002G153100	SbTGA6.7g SbTGA7	07 02	6 413 340‒ 6 427 344 45 762 133‒45 770 211	14 005 8 078
Sobic.010G192366	SbTGA8	10	53 452 812‒53 453 964	1 152
Sobic.004G078800	SbTGA9	04	6 496 341‒6 505 629	9 288
Sobic.001G243800	SbTGA10	01	25 331 187‒25 332 625	1 438

蛋白 Protein	氨基酸数目 Number of amino acids	分子量 Molecular weigh （Da）	等电点 Theoretical pI	不稳定系数 Instability index	脂溶系数 Aliphatic index	亲水性均值 Average hydrophilicity	亚细胞定位 Subcellular localization
SbTGA1.3g	468	51 130.35	6.39	55.59	77.50	-0.498	细胞核Nucleus
SbTGA1.9g	332	36 982.68	6.43	58.95	84.22	-0.519	细胞核Nucleus
SbTGA2.1a	500	55 731.81	6.91	68.96	75.00	-0.561	细胞核Nucleus
SbTGA2.1b	333	37 184.12	8.90	55.31	85.11	-0.515	细胞核Nucleus
SbTGA2.2	335	37 433.39	8.92	54.43	81.67	-0.532	细胞核Nucleus
SbTGA2.3	330	36 580.06	7.88	57.45	79.64	-0.583	细胞核Nucleus
SbTGA3	462	50 093.64	6.34	53.46	81.60	-0.110	细胞核Nucleus
SbTGA4.5g	488	53 416.73	6.13	53.23	72.38	-0.458	细胞核Nucleus
SbTGA4.8g	483	52 724.80	6.15	46.42	71.28	-0.480	细胞核Nucleus
SbLG2	533	57 914.08	6.26	53.50	75.65	-0.379	细胞核Nucleus
SbTGA5	520	56 977.68	5.83	64.27	72.60	-0.456	细胞核Nucleus
SbTGA6.6g	408	45 366.65	6.29	49.07	78.09	-0.375	细胞核Nucleus
SbTGA6.7g	516	56 764.99	9.05	49.25	86.18	-0.150	细胞核Nucleus
SbTGA7	409	45 255.64	8.46	59.10	84.01	-0.361	细胞核Nucleus
SbTGA8	158	17 172.66	5.93	52.20	89.11	-0.055	细胞核Nucleus
SbTGA9	487	52 197.54	8.55	56.19	70.99	-0.456	细胞核Nucleus
SbTGA10	311	34 461.24	8.80	50.33	88.30	-0.341	细胞核Nucleus

蛋白 Protein	氨基酸数目 Number of amino acids	分子量 Molecular weigh （Da）	等电点 Theoretical pI	不稳定系数 Instability index	脂溶系数 Aliphatic index	亲水性均值 Average hydrophilicity	亚细胞定位 Subcellular localization
SbTGA1.3g	468	51 130.35	6.39	55.59	77.50	-0.498	细胞核Nucleus
SbTGA1.9g	332	36 982.68	6.43	58.95	84.22	-0.519	细胞核Nucleus
SbTGA2.1a	500	55 731.81	6.91	68.96	75.00	-0.561	细胞核Nucleus
SbTGA2.1b	333	37 184.12	8.90	55.31	85.11	-0.515	细胞核Nucleus
SbTGA2.2	335	37 433.39	8.92	54.43	81.67	-0.532	细胞核Nucleus
SbTGA2.3	330	36 580.06	7.88	57.45	79.64	-0.583	细胞核Nucleus
SbTGA3	462	50 093.64	6.34	53.46	81.60	-0.110	细胞核Nucleus
SbTGA4.5g	488	53 416.73	6.13	53.23	72.38	-0.458	细胞核Nucleus
SbTGA4.8g	483	52 724.80	6.15	46.42	71.28	-0.480	细胞核Nucleus
SbLG2	533	57 914.08	6.26	53.50	75.65	-0.379	细胞核Nucleus
SbTGA5	520	56 977.68	5.83	64.27	72.60	-0.456	细胞核Nucleus
SbTGA6.6g	408	45 366.65	6.29	49.07	78.09	-0.375	细胞核Nucleus
SbTGA6.7g	516	56 764.99	9.05	49.25	86.18	-0.150	细胞核Nucleus
SbTGA7	409	45 255.64	8.46	59.10	84.01	-0.361	细胞核Nucleus
SbTGA8	158	17 172.66	5.93	52.20	89.11	-0.055	细胞核Nucleus
SbTGA9	487	52 197.54	8.55	56.19	70.99	-0.456	细胞核Nucleus
SbTGA10	311	34 461.24	8.80	50.33	88.30	-0.341	细胞核Nucleus

基因 Gene	非同义突变率 Ka	同义突变率 Ks	Ka/Ks
SbTGA1.3g	0.026 806	0.110 230	0.143 179
SbTGA1.9g	0.031 715	0.119 848	0.164 627
SbTGA2.1a	0.013 625	0.122 884	0.110 880
SbTGA2.1b	0.022 205	0.125 714	0.098 377
SbTGA2.2	0.010 432	0.115 926	0.089 984
SbTGA2.3	0.005 987	0.165 411	0.036 197
SbTGA3	0.046 521	0.140 532	0.331 034
SbTGA4.5g	0.018 687	0.193 302	0.096 673
SbTGA4.8g	0.056 425	0.168 138	0.110 432
SbLG2	0.024 716	0.120 180	0.104 636
SbTGA5	0.026 103	0.303 343	0.086 050
SbTGA6.6g	0.042 216	0.169 735	0.148 720
SbTGA6.7g	0.055 926	0.198 823	0.181 286
SbTGA7	0.028 116	0.142 082	0.197 886
SbTGA8	0.051 141	0.111 611	0.458 203
SbTGA9	0.070 751	0.182 973	0.386 674
SbTGA10	0.081 083	0.104 734	0.396 043

高粱TGA基因响应孢堆黑粉菌（Sporisorium reilianum）侵染表达和DNA变异分析

Analysis on Expression and DNA Variation of TGA Genes in Sorghum （Sorghum bicolor） in Response to Sporisorium reilianum Infection

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高粱品种 Sorghum variety	发病率 Incidence （%）	抗感病性表现 Disease resistance-susceptibility manifestation
7050B	0	免疫 Immunity
R111	5	抗病 Disease resistance
JL5	13	感病 Susceptibility
1383x7050B_F4-12R	0	免疫 Immunity
1383x7050B_F4-12S	75	感病 Susceptibility

基因 Gene	染色体位置 Chromosome location	Ref	Alt	注释 Effect	密码子变化 Codon change	突变种质 Mutated germplasm
SbTGA2.1a	SBI-02：63499982	A	G	NON_SYNONYMOUS_CODING	Agc/Ggc	EBA-3，2457A3，4003，91SPbigspike，Jinliang5，R111，E35B，Sp42，2457B，Pin626，Xinliang7
SbTGA6.6g	SBI-06：58476073	G	A	NON_SYNONYMOUS_CODING	Gca/Aca	C1-1-1，C1-1
SbTGA6.7g	SBI-07：6376608	A	G	NON_SYNONYMOUS_CODING	Aac/Gac	1383-2/15，EBA-3，3030，C1-1-1，44B，2457A3，91SPbigspike，Jinliang5，B35，V4A2，5-27A3R，R111，2083，2457B，3chi3 Mid，C1-1，961541H，Pin626，JF1，4003，961541，Xinliang7
SbTGA6.7g	SBI-07：6377395	C	A	NON_SYNONYMOUS_CODING	gCc/gAc	1383-2/15，EBA-3，3030，C1-1-1，2457A3，4003，91SPbigspike，Jinliang5，5-27A3R，R111，2083，2457B，3chi3 Mid，C1-1，961541H，Pin626，JF1，Xinliang7
SbTGA6.7g	SBI-07：6376406	C	G	NON_SYNONYMOUS_CODING	gCc/gGc	44B，V4A2，E35B
SbTGA6.7g	SBI-07：6376868	G	A	NON_SYNONYMOUS_CODING	cGc/cAc	44B，V4A2
SbTGA6.7g	SBI-07：6377004	C	A	NON_SYNONYMOUS_CODING	Cag/Aag	44B，V4A2，E35B
SbTGA9	SBI-04：6519320	G	C	NON_SYNONYMOUS_CODING	gGc/gCc	EBA-3，2083
SbTGA9	SBI-04：6520803	G	C	NON_SYNONYMOUS_CODING	gaG/gaC	C1-1-1，E35B，C1-1
SbTGA10	SBI-01：25344152	C	T	NON_SYNONYMOUS_CODING	Cgg/Tgg	3030，C1-1-1
SbTGA10	SBI-01：25343897	G	C	NON_SYNONYMOUS_CODING	Gcg/Ccg	V4A2，E35B

基因 Gene	染色体位置 Chromosome location	Ref	Alt	注释 Effect	突变种质 Mutated germplasm
SbTGA2.1a	SBI-02：634 999 23	cac	caGc	FRAME_SHIFT	ALL
SbTGA6.6g	SBI-06：584 754 88	cag	CCAcag	CODON_INSERTION	ALL
SbTGA6.7g	SBI-07：637 743 2	ccg	ccgCCGCCGCCGCCG	CODON_INSERTION	1383-2/15，EBA-3，3030，C1-1-1，44B，2457A3，91SPbigspike，Jinliang5，B35，V4A2，5-27A3R，R111，2083，Sp42，2457B，3chi3 Mid，C1-1，961541H，Pin626，JF1，4003，Xinliang7
SbTGA6.7g	SBI-07：637 692 5	ggagtc	gtc	CODON_DELETION	EBA-3，3030，C1-1-1，44B，2457A3，91SPbigspike，Jinliang5，V4A2，5-27A3R，R111，2083，Sp42，2457B，3chi3 Mid，C1-1，961541H，Pin626，SP91dw，E35B，JF1，4003，Xinliang7
SbTGA10	SBI-01：253 434 10	gaa	gaGGa	FRAME_SHIFT	1383-2/15，EBA-3，3030，C1-1-1，2457A3，91SPbigspike，Jinliang5，B35，V4A2，5-27A3R，R111，Sp42，SP91dw，2457B，3chi3 Mid，C1-1，961541H，Pin626，JF1，4003，Xinliang7
SbTGA10	SBI-01：253 433 88	acg	_	CODON_DELETION	1383-2/15，EBA-3，3030，C1-1-1，2457A3，91SPbigspike，Jinliang5，V4A2，5-27A3R，Sp42，SP91dw，2457B，3chi3 Mid，961541H，Pin626，JF1，4003，Xinliang7

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