番茄WRKY转录因子比较鉴定及细菌胁迫响应

水德聚; 孙继; 熊自立; 徐焕文; 张圣美; 史建磊

doi:10.19303/j.issn.1008-0384.2023.03.004

番茄WRKY转录因子比较鉴定及细菌胁迫响应

doi: 10.19303/j.issn.1008-0384.2023.03.004

温州科技职业学院/浙南作物育种重点实验室，浙江　温州　325006

基金项目: 浙江省农业新品种选育重大科技专项子课题（2021C02065）；浙江省农业高质量发展专项（浙种〔 2021〕58号）；温州市农业新品种选育协作组项目（2019ZX007）

详细信息

作者简介:
水德聚（1984−），男，硕士，主要从事蔬菜栽培与遗传育种研究（E-mail：shuidj163@163.com）

通讯作者:
史建磊（1982−），男，博士，副教授，主要从事作物遗传育种与生物技术研究（E-mail：sjlhebau@163.com）

中图分类号: S641.2
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出版历程
- 收稿日期: 2022-10-25
- 修回日期: 2023-01-30
- 网络出版日期: 2023-03-28
- 刊出日期: 2023-03-28

Identification and Pathogenic Response of Tomato WRKY Transcription Factors

Southern Zhejiang Key Laboratory of Crop Breeding, Wenzhou Vocational College of Science and Technology, Wenzhou, Zhejiang　325006, China

摘要

摘要: 目的深入了解番茄WRKY转录因子的组学特征及其生物胁迫响应。方法基于最新公共数据，利用生物信息学和比较基因组学方法对番茄WRKY进行系统鉴定，结合抗、感2个番茄自交系在青枯菌侵染前后的RNA-seq数据，挖掘青枯病抗性相关WRKY。结果 85个番茄WRKY转录因子被鉴定，可分为I、IIa+b、IIc、IId+e和III等类别，IIe基因最多。其中，9个基因七肽基序发生了单一氨基酸变异，WRKYGKK为优势突变型。这些WRKY主要分布在5号染色体，且具有端部和成簇分布现象，尤其是IIe亚类。45.88%的番茄WRKY具有共线性。58.82%的番茄WRKY（主要是I和IIc类）与拟南芥和辣椒WRKY形成73对直系同源基因，其选择压力（Ka/Ks）均小于1。16个番茄WRKY（主要是IIa+b和IIc类）对几种生物胁迫反应强烈，且主要在根中表达。12个差异表达WRKY（主要是III和IIb类）被鉴定，其中Solyc03g095770.3（III）与Solyc09g014990.4（I）互作在番茄青枯病响应中发挥重要作用。结论综合鉴定了番茄WRKY转录因子，筛选到12个青枯病响应基因。
- 番茄 /
- WRKY转录因子 /
- 基因特征 /
- 生物胁迫 /
- 转录表达
Abstract: Objective Characteristics and biotic stress response of WRKY transcription factors (TFs) in tomato plants were investigated. Method The latest available bioinformatics and genomics methods were employed to identify the tomato WRKY TFs. RNA-seq of disease-resistant and susceptible tomato inbred lines before and after artificial Ralstonia solanacearum infection were obtained to identify the TFs associated with the pathogenic resistance of the plants. Result Eighty-five tomato WRKY TFs were identified and divided into I, IIa+b, IIc, IId+e, and III categories. The IIe group had the highest number of the TFs. The conserved motif of 9 TFs had one single amino acid variation, and WRKYGKK was the dominant mutant. The TFs, especially those in the IIe group, were mainly found on chromosome 5, at the ends, and in clusters. In them, 45.88% showed collinearity and 58.82% (mainly in I and IIc groups) formed 73 pairs of orthologs with those in Arabidopsis and chili pepper at a Ka/Ks ratio below 1. Sixteen of them, mainly belonging to IIa+b and IIc, responded significantly to the biotic stress with expressions largely in the roots. There were 12 differentially expressed WRKY TFs identified mainly in III and IIb. Of which, the interaction between Solyc03g095770.3 (III) and Solyc09g014990.4 (I) played a significant role in the response of the tomato plant to bacterial wilt. Conclusion The WRKY TFs were identified in tomato plants. Twelve genes responded to the bacterial wilt were isolated.
- Tomato /
- WRKY transcription factor /
- genetic characteristics /
- biotic stress /
- transcriptional expression

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图 1 番茄WRKY转录因子保守序列

Figure 1. Conserved sequences of WRKY TFs in tomato

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图 2 番茄WRKY转录因子种内共线性

Figure 2. Intraspecific collinearity of WRKY TFs in tomato

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图 3 番茄、辣椒和拟南芥WRKY转录因子系统发生树

氨基酸多序列比对后，用IQ-Tree基于最大似然法构建系统发生树。红色标注指图位克隆到的首个抗青枯病基因RRS1。

Figure 3. Phylogenetic trees of WRKY TFs in tomato, chili pepper and Arabidopsis

IQ-Tree based on maximum likelihood (ML) method after multiple amino acid sequence alignment was used to construct phylogenetic tree. Red indicates 1^st bacterial wilt resistance gene RRS1 from map-based cloning.

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图 4 番茄WRKY在不同组织部位（a）和病菌侵染（b）下的相对表达

a: 栽培番茄Heinz1706，1. 芽，2. 花，3. 叶，4. 根，5~7. 果（1~3 cm），8. 绿熟期，9. 破色期，10. 破色后10 d；醋栗番茄（S. pimpinellifolium），11. 绿果期，12. 破色期，13. 破色后5 d，14. 叶。b：1. 细菌鞭毛蛋白/对照病原相关分子模式 6 h，2~4. 不同丁香假单胞菌/对照细菌 6 h，5. 荧光假单胞菌/对照细菌 6 h，6. 恶臭假单胞菌/对照细菌 6 h，7. 根癌农杆菌/对照细菌 6 h。

Figure 4. Expression profiles of WRKY TFs in different tissues (a) and with pathogen infection (b) in tomato

a: cultivated tomato Heinz1706, 1. bud, 2. flower, 3. leaf, 4. root, 5–7. fruit (1-3 cm), 8. mature green (MG), 9. breaker (B), 10. breaker+10 (B10); wild S. pimpinellifolium, 11. immature green (IM), 12. breaker (B), 13. breaker+5 (B5), 14. leaf. b: 1. flagellin (flgII-28)/mock pathogen-associated molecular pattern (PAMP) 6 h, 2-4. different Pseudomonas syringae strains (DC3000, DC3000ΔhrcQ-UΔfliC, and DC3000ΔAvrPtoΔAvrPtoB)/bacterial mock 6 h, 5. Pseudomonas fluorescens/bacterial mock 6 h, 6. Pseudomonas putida/bacterial mock 6 h, and 7. Agrobacterium tumefaciens/bacterial mock 6 h.

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图 5 番茄WRKY转录因子间的互作

红色和绿色圆圈分别代表正负调控基因。圆圈大小表示互作因子数量，连接线宽度表示互作强度。

Figure 5. Interactions among WRKY TFs in tomato

Red and green circles represent positively and negatively regulated genes, respectively; size of circle, number of interacting factors; thickness of gray line, interaction strength.

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表 1 番茄WRKY转录因子基因家族

Table 1. WRKY TF gene family in tomato

基因 ID Gene ID	AA	MW/kD	pI	II	SL	基因 ID Gene ID	AA	MW/kD	pI	II	SL
Solyc01g058540.3	324	35.49	4.74	72.92	nucl	Solyc05g050060.1	322	36.76	9.23	56.65	nucl
Solyc01g079260.4	347	39.15	6.45	40.95	extr	Solyc05g050065.1	126	14.62	9.11	58.95	nucl
Solyc01g079360.4	240	26.88	5.03	49.87	nucl	Solyc05g050300.3	195	22.57	6.06	53.10	cyto
Solyc01g089960.3	288	32.57	8.60	46.70	nucl	Solyc05g050330.3	244	27.54	6.02	54.36	nucl
Solyc01g095100.4	315	34.95	6.50	63.97	nucl	Solyc05g050340.4	218	24.58	5.05	46.20	nucl
Solyc01g095630.3	336	37.73	5.55	58.66	nucl	Solyc05g053380.4	304	34.36	7.75	56.40	nucl
Solyc01g104550.3	475	52.98	6.09	50.54	nucl	Solyc05g055750.3	459	51.65	8.77	45.35	nucl
Solyc02g021680.3	381	42.63	5.37	47.45	nucl	Solyc06g008610.3	348	39.05	9.64	53.70	nucl
Solyc02g032950.3	504	56.31	8.17	49.81	nucl	Solyc06g048870.3	243	26.85	6.15	38.10	nucl
Solyc02g067430.3	440	48.40	6.99	60.86	nucl	Solyc06g066370.4	549	61.30	6.72	60.62	vacu
Solyc02g071130.4	329	37.85	6.55	55.76	nucl	Solyc06g068460.3	360	39.74	8.37	43.78	nucl
Solyc02g072190.4	304	33.99	6.29	70.76	nucl	Solyc06g070990.3	649	71.66	6.07	52.36	nucl
Solyc02g080890.3	550	59.66	7.25	45.54	nucl	Solyc07g005650.4	513	56.29	6.41	56.26	nucl
Solyc02g088340.4	460	50.95	6.20	59.45	nucl	Solyc07g047960.3	420	45.96	6.93	69.06	nucl
Solyc02g093050.3	326	36.21	9.65	48.66	nucl	Solyc07g051840.4	660	72.08	6.32	50.50	nucl
Solyc02g094270.2	131	15.47	9.51	35.84	cyto	Solyc07g055280.4	275	29.90	5.48	55.13	nucl
Solyc03g007380.2	353	40.06	6.09	51.86	nucl	Solyc07g056280.3	322	36.65	6.00	61.72	nucl
Solyc03g007640.1	359	41.14	6.98	64.88	nucl	Solyc07g065260.4	601	65.55	6.58	49.22	nucl
Solyc03g082750.1	178	20.73	9.64	38.54	chlo	Solyc07g066220.3	739	79.85	6.04	51.97	nucl
Solyc03g082810.1	219	25.05	6.55	43.49	nucl	Solyc08g006320.4	335	36.44	9.70	37.80	nucl
Solyc03g095770.3	273	31.53	6.02	55.04	nucl	Solyc08g008280.3	360	40.71	5.51	47.00	nucl
Solyc03g104810.3	486	53.90	6.83	66.50	nucl	Solyc08g067340.4	279	31.95	9.31	50.58	nucl
Solyc03g113120.4	530	58.87	6.83	43.04	nucl	Solyc08g067360.3	258	29.35	5.60	51.10	nucl
Solyc03g116890.3	350	39.18	8.73	48.24	nucl	Solyc08g081610.4	303	34.69	5.49	56.18	nucl
Solyc04g050205.1	117	13.73	9.54	44.50	cyto	Solyc08g081630.2	231	26.41	8.97	56.81	pero
Solyc04g050210.1	366	41.61	5.25	51.49	nucl	Solyc08g082110.4	380	43.45	6.82	45.73	chlo
Solyc04g051540.3	237	27.14	8.74	57.58	nucl	Solyc09g010960.3	290	32.37	5.27	48.26	nucl
Solyc04g051690.4	174	19.96	7.05	40.62	nucl	Solyc09g014990.4	529	58.67	7.66	56.35	nucl
Solyc04g056360.4	413	47.29	5.83	57.52	nucl	Solyc09g015770.3	291	33.25	5.51	60.87	nucl
Solyc04g072070.3	255	29.59	8.32	37.35	nucl	Solyc09g066010.3	331	37.30	9.66	57.28	nucl
Solyc04g078550.3	351	38.49	9.63	54.29	nucl	Solyc10g005680.2	703	76.13	5.18	47.47	nucl
Solyc05g007110.2	392	44.41	8.89	48.16	nucl	Solyc10g007970.2	255	28.60	7.07	47.03	nucl
Solyc05g012500.3	327	35.43	5.26	57.84	nucl	Solyc10g009550.3	290	33.65	5.45	50.93	nucl
Solyc05g012770.3	508	55.40	7.65	65.68	nucl	Solyc10g011910.4	348	39.17	5.97	50.91	nucl
Solyc05g014040.1	290	32.49	9.41	59.32	nucl	Solyc10g084380.1	422	46.99	9.49	70.75	nucl
Solyc05g015850.4	176	20.31	9.22	40.11	nucl	Solyc12g006170.2	549	60.45	6.24	49.52	nucl
Solyc05g045710.3	238	26.99	9.00	63.69	cyto	Solyc12g011200.3	335	37.80	5.87	63.14	nucl
Solyc05g045800.1	253	28.49	9.29	58.72	nucl	Solyc12g014610.2	611	65.94	6.23	51.69	nucl
Solyc05g045880.1	321	36.33	8.74	50.56	nucl	Solyc12g042590.2	252	28.56	8.82	38.23	nucl
Solyc05g045927.1	241	27.83	9.25	48.99	nucl	Solyc12g056745.1	324	37.80	6.33	38.64	nucl
Solyc05g050040.3	278	31.44	9.37	57.09	nucl	Solyc12g056750.3	188	22.46	8.78	24.31	nucl
Solyc05g050050.1	322	36.75	9.26	58.14	nucl	Solyc12g096350.2	338	36.94	9.75	34.56	nucl
Solyc05g050057.1	129	14.92	9.71	62.07	nucl
1）AA：氨基酸数；MW：分子量；pI：理论等电点；II：不稳定系数；SL：亚细胞定位。2）nucl：细胞核；cyto：细胞质；chlo：叶绿体；pero：过氧化物酶体；extr：胞外间隙；vacu：液泡。 1) AA: Number of amino acids; MW: molecular weight; pI: Theoretical isoelectric point; II: Instability index; SL: Subcellular localization. 2) nucl: Nucleus; cyto: Cytoplasm; chlo: Chloroplast; pero: Peroxysome; extr: Extracellular; vacu: Vacuole.

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表 2 番茄WRKY转录因子染色体分布

Table 2. Distribution of WRKY TFs in tomato chromosomes

染色体 Chromosome	基因数 Genes	基因簇 Gene clusters	成簇基因 Genes in clusters	单簇基因 Genes per cluster	成簇基因占比 Percentage/%	串联重复基因 Tandem repeat genes	重复基因占比 Percentage/%
Chr.1	7	0	0	—	0.0	0	0.0
Chr.2	9	0	0	—	0.0	0	0.0
Chr.3	8	1	2	2	25.0	0	0.0
Chr.4	7	0	0	—	0.0	0	0.0
Chr.5	19	3	12	4	63.2	9	47.4
Chr.6	5	0	0	—	0.0	0	0.0
Chr.7	7	0	0	—	0.0	0	0.0
Chr.8	7	2	4	2	57.1	2	28.6
Chr.9	4	0	0	—	0.0	0	0.0
Chr.10	5	0	0	—	0.0	0	0.0
Chr.11	0	0	0	—	—	0	—
Chr.12	7	1	2	2	28.6	2	28.6
—：表示不适用，下同。 —: Not applicable. The same below.

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表 3 番茄与辣椒、拟南芥之间的WRKY同源基因对

Table 3. WRKY homolog between tomato and chili pepper or Arabidopsis

基因1 Gene 1	基因2 Gene 2	类别 Group	Ka	Ks	Ka/Ks	基因1 Gene 1	基因2 Gene 2	类别 Group	Ka	Ks	Ka/Ks
Solyc01g079260.4	Capana01g002803	IIc	0.114	0.654	0.174	Solyc08g082110.4	Capana01g004471	III	0.268	0.970	0.276
Solyc01g089960.3	Capana01g003441	IIc	0.088	0.355	0.249	Solyc10g005680.2	Capana10g000205	I	0.236	0.283	0.834
Solyc01g095100.4	Capana08g001012	IIe	0.042	0.301	0.140	Solyc10g009550.3	Capana08g001044	III	0.331	1.184	0.279
Solyc01g095630.3	Capana08g001044	III	0.103	0.439	0.235	Solyc10g084380.1	Capana10g001791	I	0.072	0.231	0.314
Solyc01g104550.3	Capana08g001961	IIb	0.052	0.262	0.199	Solyc12g006170.2	Capana00g004057	I	0.088	0.188	0.470
Solyc02g067430.3	Capana02g000918	IIb	0.070	0.316	0.222	Solyc12g011200.3	Capana09g000676	IIc	0.071	0.228	0.310
Solyc02g072190.4	Capana02g001642	IIe	0.066	0.389	0.169	Solyc01g079260.4	AT2G47260.1	IIc	0.488	1.512	0.323
Solyc02g080890.3	Capana02g002230	IIb	0.054	0.373	0.144	Solyc01g089960.3	AT2G44745.1	IIc	0.289	2.165	0.134
Solyc02g088340.4	Capana02g003339	I	0.080	0.222	0.359	Solyc01g095100.4	AT4G01250.1	IIe	0.382	1.931	0.198
Solyc02g093050.3	Capana02g003053	IId	0.116	0.532	0.218	Solyc01g095630.3	AT2G46400.1	III	0.590	—	—
Solyc02g094270.2	Capana02g003661	IIc	0.099	0.278	0.356	Solyc02g021680.3	AT2G34830.2	IIe	0.446	—	—
Solyc03g007380.2	Capana03g002072	III	0.103	0.486	0.213	Solyc02g071130.4	AT4G18170.1	IIc	0.446	1.921	0.232
Solyc03g007640.1	Capana03g002134	IIe	0.388	0.708	0.547	Solyc02g071130.4	AT5G46350.1	IIc	0.424	2.659	0.159
Solyc03g082810.1	Capana03g001962	IIe	0.142	0.308	0.460	Solyc02g071130.4	AT1G29860.1	IIc	0.366	2.306	0.159
Solyc03g095770.3	Capana03g002635	III	0.148	0.309	0.480	Solyc02g088340.4	AT1G13960.1	I	0.382	1.643	0.233
Solyc03g113120.4	Capana03g001099	IIb	0.083	0.399	0.209	Solyc02g088340.4	AT3G01080.2	I	0.512	—	—
Solyc03g116890.3	Capana03g000473	IIa	0.102	0.455	0.224	Solyc02g094270.2	AT3G01970.1	IIc	0.384	—	—
Solyc04g051540.3	Capana12g001851	IIc	0.042	0.194	0.215	Solyc03g116890.3	AT1G80840.1	IIa	0.340	2.918	0.117
Solyc04g051690.4	Capana12g001826	IIc	0.080	0.300	0.266	Solyc05g007110.2	AT1G69810.1	IIb	0.491	—	—
Solyc04g056360.4	Capana05g002502	I	0.394	1.071	0.368	Solyc05g012500.3	AT1G69310.1	IIc	0.376	3.568	0.106
Solyc04g078550.3	Capana04g000568	IId	0.066	0.660	0.099	Solyc05g012770.3	AT1G13960.1	I	0.285	2.483	0.115
Solyc05g012500.3	Capana11g001905	IIc	0.132	0.357	0.369	Solyc05g012770.3	AT2G03340.1	I	0.290	2.177	0.133
Solyc05g012770.3	Capana11g001882	I	0.045	0.346	0.130	Solyc06g048870.3	AT2G40740.3	NG	0.389	2.044	0.190
Solyc05g055750.3	Capana05g002502	I	0.118	0.324	0.363	Solyc06g070990.3	AT1G18860.1	IIb	0.464	2.330	0.199
Solyc06g008610.3	Capana06g003072	IId	0.042	0.251	0.168	Solyc06g070990.3	AT5G15130.1	IIb	0.524	3.356	0.156
Solyc06g066370.4	Capana06g001506	I	0.032	0.261	0.123	Solyc07g047960.3	AT2G04880.1	I	0.513	2.372	0.216
Solyc06g068460.3	Capana06g001110	IIa	0.053	0.282	0.187	Solyc07g065260.4	AT4G26640.2	I	0.370	2.286	0.162
Solyc06g070990.3	Capana06g001008	IIb	0.058	0.396	0.146	Solyc08g006320.4	AT2G24570.1	IId	0.343	1.396	0.245
Solyc07g005650.4	Capana07g000181	I	0.131	0.307	0.427	Solyc08g006320.4	AT4G31550.1	IId	0.401	2.820	0.142
Solyc07g047960.3	Capana07g001256	I	0.089	0.162	0.553	Solyc08g081610.4	AT4G23550.1	IIe	0.552	—	—
Solyc07g051840.4	Capana07g001387	IIb	0.061	0.259	0.235	Solyc08g082110.4	AT4G11070.1	III	0.439	2.534	0.173
Solyc07g055280.4	Capana07g001809	IIe	0.087	0.445	0.195	Solyc08g082110.4	AT4G23810.1	III	0.436	—	—
Solyc07g056280.3	Capana07g001968	IIc	0.051	0.251	0.202	Solyc09g014990.4	AT2G38470.1	I	0.368	—	—
Solyc07g065260.4	Capana07g002350	I	0.054	0.176	0.308	Solyc10g005680.2	AT4G26440.1	I	0.524	1.613	0.325
Solyc08g008280.3	Capana01g004471	III	0.131	0.401	0.327	Solyc10g084380.1	AT2G37260.1	I	0.496	2.115	0.235
Solyc08g081610.4	Capana01g000167	IIe	0.076	0.228	0.334	Solyc12g014610.2	AT4G26640.2	I	0.394	2.070	0.190
Solyc08g081630.2	Capana01g000165	IIc	0.187	0.522	0.358

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表 4 番茄青枯菌诱导转录差异表达WRKY

Table 4. Transcriptionally DE WRKY TFs with RsI in tomato

基因ID Gene ID	类别 Group	RC_vs_RT FDR	RC_vs_RT log₂FC	SC_vs_ST FDR	SC_vs_ST log₂FC	GO/KEGG注释 GO/KEGG annotation
Solyc01g089960.3	IIc	0.00	−0.99	0.90	0.05	GO:0003700、GO:0006355、GO:0043565
Solyc01g104550.3	IIb	0.03	0.65	0.62	0.22	GO:0003700、GO:0006355、GO:0043565、GO:0044212
Solyc02g032950.3	IIb	0.01	1.05	0.19	0.49	GO:0003700、GO:0006355、GO:0043565
Solyc03g095770.3	III	0.80	0.12	0.02	0.78	GO:0003700、GO:0006355、GO:0043565
Solyc04g051540.3	IIc	0.00	−1.08	0.54	−0.24	GO:0003700、GO:0006355、GO:0043565
Solyc05g050340.4	III	0.46	0.26	0.05	0.71	GO:0003700、GO:0006355、GO:0043565
Solyc05g055750.3	I	0.91	0.06	0.02	−0.67	GO:0003700、GO:0006355、GO:0043565
Solyc07g051840.4	IIb	0.00	1.17	0.00	0.76	GO:0003700、GO:0006355、GO:0043565
Solyc09g014990.4	I	0.01	1.06	0.01	0.88	GO:0003700、GO:0006355、GO:0043565、ko04626
Solyc09g015770.3	III	0.20	0.61	0.00	1.44	GO:0003700、GO:0006355、GO:0043565
Solyc09g066010.3	IId	0.37	−0.24	0.00	−0.66	GO:0003700、GO:0006355、GO:0043565
Solyc10g009550.3	III	0.00	1.18	0.00	0.90	GO:0003700、GO:0006355、GO:0043565
R和S分别代表抗病和感病番茄自交系，C和T分别代表对照和青枯菌侵染。GO:0003700表示转录因子活性和序列特异性DNA结合，GO:0006355表示转录调控，GO:0043565表示序列特异性DNA结合，GO:0044212表示转录调控区DNA结合，ko04626表示植物-病原互作。 R and S: resistant and susceptible tomato inbred lines, respectively; C: control; T: RsI. GO:0003700: transcription factor activity and sequence-specific DNA binding; GO:0006355: regulation of transcription; GO:0043565: sequence-specific DNA binding; GO:0044212: transcription regulatory region DNA binding; ko04626: plant-pathogen interaction.

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参考文献(46)

[1]	刘强, 张贵友, 陈受宜. 植物转录因子的结构与调控作用 [J]. 科学通报, 2000, 45(14):1465−1474. doi: 10.3321/j.issn:0023-074X.2000.14.002 LIU Q, ZHANG G Y, CHEN S Y. Structure and regulation of plant transcription factors [J]. Chinese Science Bulletin, 2000, 45(14): 1465−1474.(in Chinese) doi: 10.3321/j.issn:0023-074X.2000.14.002
[2]	RUSHTON P J, SOMSSICH I E, RINGLER P, et al. WRKY transcription factors [J]. Trends in Plant Science, 2010, 15(5): 247−258. doi: 10.1016/j.tplants.2010.02.006
[3]	EULGEM T, RUSHTON P J, ROBATZEK S, et al. The WRKY superfamily of plant transcription factors [J]. Trends in Plant Science, 2000, 5(5): 199−206. doi: 10.1016/S1360-1385(00)01600-9
[4]	AGARWAL P, REDDY M P, CHIKARA J. WRKY: Its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants [J]. Molecular Biology Reports, 2011, 38(6): 3883−3896. doi: 10.1007/s11033-010-0504-5
[5]	赵楠楠, 刘立峰. 植物WRKY转录因子及其生物学功能 [J]. 分子植物育种, 2019, 17(21):7040−7046. doi: 10.13271/j.mpb.017.007040 ZHAO N N, LIU L F. WRKY transcription factors and their biological functions in plants [J]. Molecular Plant Breeding, 2019, 17(21): 7040−7046.(in Chinese) doi: 10.13271/j.mpb.017.007040
[6]	XIE Z, ZHANG Z L, ZOU X L, et al. Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells [J]. Plant Physiology, 2005, 137(1): 176−189. doi: 10.1104/pp.104.054312
[7]	BAKSHI M, OELMÜLLER R. WRKY transcription factors: Jack of many trades in plants [J]. Plant Signaling & Behavior, 2014, 9(2): e27700.
[8]	WU K L, GUO Z J, WANG H H, et al. The WRKY family of transcription factors in rice and Arabidopsis and their origins [J]. DNA Research, 2005, 12(1): 9−26. doi: 10.1093/dnares/12.1.9
[9]	ZHANG Y J, WANG L J. The WRKY transcription factor superfamily: Its origin in eukaryotes and expansion in plants [J]. BMC Evolutionary Biology, 2005, 5(1): 1. doi: 10.1186/1471-2148-5-1
[10]	CHEN L G, SONG Y, LI S J, et al. The role of WRKY transcription factors in plant abiotic stresses [J]. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 2012, 1819(2): 120−128. doi: 10.1016/j.bbagrm.2011.09.002
[11]	ROSS C A, LIU Y, SHEN Q J. The WRKY gene family in rice (Oryza sativa) [J]. Journal of Integrative Plant Biology, 2007, 49(6): 827−842. doi: 10.1111/j.1744-7909.2007.00504.x
[12]	WEI K F, CHEN J, CHEN Y F, et al. Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize [J]. DNA Research, 2012, 19(2): 153−164. doi: 10.1093/dnares/dsr048
[13]	BENCKE-MALATO M, CABREIRA C, WIEBKE-STROHM B, et al. Genome-wide annotation of the soybean WRKY family and functional characterization of genes involved in response to Phakopsora pachyrhizi infection [J]. BMC Plant Biology, 2014, 14: 236. doi: 10.1186/s12870-014-0236-0
[14]	ZHANG C, WANG D D, YANG C H, et al. Genome-wide identification of the potato WRKY transcription factor family [J]. PLoS One, 2017, 12(7): e0181573. doi: 10.1371/journal.pone.0181573
[15]	HUANG S X, GAO Y F, LIU J K, et al. Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum [J]. Molecular Genetics and Genomics, 2012, 287(6): 495−513. doi: 10.1007/s00438-012-0696-6
[16]	YANG Y, LIU J, ZHOU X H, et al. Identification of WRKY gene family and characterization of cold stress-responsive WRKY genes in eggplant [J]. PeerJ, 2020, 8: e8777. doi: 10.7717/peerj.8777
[17]	SCIENCE F I P. Retraction: Genome-wide identification and expression analysis of WRKY gene family in Capsicum annuum L [J]. Frontiers in Plant Science, 2016, 7: 1727.
[18]	LING J, JIANG W J, ZHANG Y, et al. Genome-wide analysis of WRKY gene family in Cucumis sativus [J]. BMC Genomics, 2011, 12: 471. doi: 10.1186/1471-2164-12-471
[19]	PHUKAN U J, JEENA G S, SHUKLA R K. WRKY transcription factors: Molecular regulation and stress responses in plants [J]. Frontiers in Plant Science, 2016, 7: 760.
[20]	史建磊, 熊自立, 苏世闻, 等. 基于RNA-seq的番茄青枯病响应基因鉴定与表达分析 [J]. 华北农学报, 2022, 37(2):171−182. doi: 10.7668/hbnxb.20192621 SHI J L, XIONG Z L, SU S W, et al. Identification and expression analysis of bacterial wilt response genes based on RNA-seq in tomato [J]. Acta Agriculturae Boreali-Sinica, 2022, 37(2): 171−182.(in Chinese) doi: 10.7668/hbnxb.20192621
[21]	CHEN C J, CHEN H, ZHANG Y, et al. TBtools: An integrative toolkit developed for interactive analyses of big biological data [J]. Molecular Plant, 2020, 13(8): 1194−1202. doi: 10.1016/j.molp.2020.06.009
[22]	ASHBURNER M, BALL C A, BLAKE J A, et al. Gene Ontology: Tool for the unification of biology [J]. Nature Genetics, 2000, 25(1): 25−29. doi: 10.1038/75556
[23]	KANEHISA M, GOTO S, KAWASHIMA S, et al. The KEGG resource for deciphering the genome [J]. Nucleic Acids Research, 2004, 32(Suppl_1): D277−D280.
[24]	LEE S W, HAN S W, SRIRIYANUM M, et al. A type I–secreted, sulfated peptide triggers XA21-mediated innate immunity [J]. Science, 2009, 326(5954): 850−853. doi: 10.1126/science.1173438
[25]	张红, 姜景彬, 许向阳, 等. 番茄WRKY基因家族的生物信息学分析 [J]. 分子植物育种, 2016, 14(8):1965−1976. doi: 10.13271/j.mpb.014.001965 ZHANG H, JIANG J B, XU X Y, et al. Bioinformatics analysis of WRKY gene family in tomato [J]. Molecular Plant Breeding, 2016, 14(8): 1965−1976.(in Chinese) doi: 10.13271/j.mpb.014.001965
[26]	SONG H, SUN W H, YANG G F, et al. WRKY transcription factors in legumes [J]. BMC Plant Biology, 2018, 18(1): 243. doi: 10.1186/s12870-018-1467-2
[27]	MOHANTA T K, PARK Y H, BAE H H. Novel genomic and evolutionary insight of WRKY transcription factors in plant lineage [J]. Scientific Reports, 2016, 6(1): 1−22. doi: 10.1038/s41598-016-0001-8
[28]	CHEN F, HU Y, VANNOZZI A, et al. The WRKY transcription factor family in model plants and crops [J]. Critical Reviews in Plant Sciences, 2017, 36(5/6): 311−335.
[29]	刁卫平, 王述彬, 刘金兵, 等. 辣椒全基因组WRKY转录因子的分析 [J]. 园艺学报, 2015, 42(11):2183−2196. DIAO W P, WANG S B, LIU J B, et al. Genome-wide analysis of the WRKY transcription factor family in pepper [J]. Acta Horticulturae Sinica, 2015, 42(11): 2183−2196.(in Chinese)
[30]	LIU J L, LIU X L, DAI L Y, et al. Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants [J]. Journal of Genetics and Genomics, 2007, 34(9): 765−776. doi: 10.1016/S1673-8527(07)60087-3
[31]	ÜLKER B, SOMSSICH I E. WRKY transcription factors: From DNA binding towards biological function [J]. Current Opinion in Plant Biology, 2004, 7(5): 491−498. doi: 10.1016/j.pbi.2004.07.012
[32]	RINERSON C I, RABARA R C, TRIPATHI P, et al. The evolution of WRKY transcription factors [J]. BMC Plant Biology, 2015, 15: 66. doi: 10.1186/s12870-015-0456-y
[33]	DESLANDES L, OLIVIER J, THEULIERES F, et al. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes [J]. Proceedings of the National Academy of Sciences of the United States of America, 2002, 99(4): 2404−2409. doi: 10.1073/pnas.032485099
[34]	MUKHTAR M S, DESLANDES L, AURIAC M C, et al. The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum [J]. The Plant Journal, 2008, 56(6): 935−947. doi: 10.1111/j.1365-313X.2008.03651.x
[35]	DANG F F, WANG Y N, YU L, et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection [J]. Plant, Cell & Environment, 2013, 36(4): 757−774.
[36]	CAI H Y, YANG S, YAN Y, et al. CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper [J]. Journal of Experimental Botany, 2015, 66(11): 3163−3174. doi: 10.1093/jxb/erv125
[37]	HUSSAIN A, LI X, WENG Y H, et al. CaWRKY22 acts as a positive regulator in pepper response to RalstoniaSolanacearum by constituting networks with CaWRKY6, CaWRKY27, CaWRKY40, and CaWRKY58 [J]. International Journal of Molecular Sciences, 2018, 19(5): 1426. doi: 10.3390/ijms19051426
[38]	DANG F F, WANG Y N, SHE J J, et al. Overexpression of CaWRKY27, a subgroup IIe WRKY transcription factor of Capsicum annuum, positively regulates tobacco resistance to Ralstonia solanacearum infection [J]. Physiologia Plantarum, 2014, 150(3): 397−411. doi: 10.1111/ppl.12093
[39]	YANG S, ZHANG Y W, CAI W W, et al. CaWRKY28 Cys249 is required for interaction with CaWRKY40 in the regulation of pepper immunity to Ralstonia solanacearum [J]. Molecular Plant-Microbe Interactions:MPMI, 2021, 34(7): 733−745. doi: 10.1094/MPMI-12-20-0361-R
[40]	HUSSAIN A, KHAN M I, ALBAQAMI M, et al. CaWRKY30 positively regulates pepper immunity by targeting CaWRKY40 against Ralstonia solanacearum inoculation through modulating defense-related genes [J]. International Journal of Molecular Sciences, 2021, 22(21): 12091. doi: 10.3390/ijms222112091
[41]	IFNAN KHAN M, ZHANG Y W, LIU Z Q, et al. CaWRKY40b in pepper acts as a negative regulator in response to Ralstonia solanacearum by directly modulating defense genes including CaWRKY40 [J]. International Journal of Molecular Sciences, 2018, 19(5): 1403. doi: 10.3390/ijms19051403
[42]	WANG Y N, DANG F F, LIU Z Q, et al. CaWRKY58, encoding a group WRKY transcription factor of Capsicum annuum, negatively regulates resistance to Ralstonia solanacearum infection [J]. Molecular Plant Physiology, 2013, 14(2): 131−144.
[43]	谢政文, 王连军, 陈锦洋, 等. 植物WRKY转录因子及其生物学功能研究进展 [J]. 中国农业科技导报, 2016, 18(3):46−54. doi: 10.13304/j.nykjdb.2015.605 XIE Z W, WANG L J, CHEN J Y, et al. Studies on WRKY transcription factors and their biological functions in plants [J]. Journal of Agricultural Science and Technology, 2016, 18(3): 46−54.(in Chinese) doi: 10.13304/j.nykjdb.2015.605
[44]	CHENG Y, ZHOU Y, YANG Y, et al. Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors [J]. Plant Physiology, 2012, 159(2): 810−825. doi: 10.1104/pp.112.196816
[45]	PARK C Y, LEE J H, YOO J H, et al. WRKY group IId transcription factors interact with calmodulin [J]. FEBS Letters, 2005, 579(6): 1545−1550. doi: 10.1016/j.febslet.2005.01.057
[46]	黄幸, 丁峰, 彭宏祥, 等. 植物WRKY转录因子家族研究进展 [J]. 生物技术通报, 2019, 35(12):129−143. doi: 10.13560/j.cnki.biotech.bull.1985.2019-0626 HUANG X, DING F, PENG H X, et al. Research progress on family of plant WRKY transcription factors [J]. Biotechnology Bulletin, 2019, 35(12): 129−143.(in Chinese) doi: 10.13560/j.cnki.biotech.bull.1985.2019-0626