CaWRKY27通过调控CaPR1和CaPR1L的表达介导辣椒对青枯菌的免疫

doi:10.16420/j.issn.0513-353x.2025-0080

摘要/Abstract

摘要：

植物特异性转录因子WRKY在调控水杨酸（salicylic acid，SA）介导的免疫中发挥着重要作用，CaWRKY27是CaWRKYⅡe亚家族成员，调控辣椒（Capsicum annuum L.）对青枯病的抗性。为了进一步解析CaWRKY27在辣椒抗青枯病中的作用机制，共鉴定出辣椒基因组中的5个CaWRKYⅡe亚家族成员。系统进化树和氨基酸序列比对分析显示，CaWRKY27与番茄SlWRKY79、拟南芥AtWRKY65同源性较高。实时荧光定量PCR（RT-qPCR）分析表明，在接种青枯菌24和48 h后，CaWRKY27沉默株系中病程相关基因CaPR1和CaPR1L的表达量显著低于对照株系。双荧光素报告实验和凝胶阻滞实验表明，CaWRKY27可直接与CaPR1和CaPR1L的启动子中的W-box元件结合并激活其表达。上述结果表明，辣椒CaWRKY27通过直接调控SA信号途径相关基因CaPR1和CaPR1L的表达从而正调控辣椒对青枯病的抗性。

关键词: 辣椒, CaWRKY27, 转录因子, 青枯病, 病程相关基因, W-box, 水杨酸（SA）信号途径

Abstract:

The WRKY transcription factors，which are specific to plants，play a crucial role in regulating salicylic acid（SA）-mediated immune response. CaWRKY27，a member of the CaWRKYⅡe subfamily，is implicated in modulating the resistance of pepper plants to bacterial wilt. To further elucidate the mechanism of action of CaWRKY27 gene in pepper’s resistance to bacterial wilt，five members of the CaWRKYⅡe subfamily were identified within the pepper genome. Phylogenetic analysis and multiple amino acid sequence alignment revealed that CaWRKY27 exhibits a high degree of homology with SlWRKY79 from tomato and AtWRKY65 from Arabidopsis. Real-time quantitative PCR（RT-qPCR）analysis demonstrated that the expression levels of the pathogenesis-related genes CaPR1 and CaPR1L were significantly reduced in pTRV2-CaWRKY27（CaWRKY27 silencing）plants compared to at both 24 and 48 hours post-inoculation with Ralstonia solanacearum in pepper. Furthermore，both dual-luciferase reporter（DLR）assays and electrophoretic mobility shift assays（EMSA）revealed that CaWRKY27 can directly bind to the W-box in the promoters of the CaPR1 and CaPR1L genes，thereby activating their expression. These findings indicate that CaWRKY27 plays a crucial role in the resistance to bacterial wilt by directly regulating the expression of SA signaling pathway-related genes CaPR1 and CaPR1L in pepper.

Key words: pepper, CaWRKY27, transcription factor, bacterial wilt, pathogenesis-related genes, W-box, SA signaling pathway

折建局, 田雅珊, 陈风, 党峰峰. CaWRKY27通过调控CaPR1和CaPR1L的表达介导辣椒对青枯菌的免疫[J]. 园艺学报, 2026, 53(3): 831-844.

SHE Jianju, TIAN Yashan, CHEN Feng, DANG Fengfeng. CaWRKY27 Mediates Pepper Immunity to Ralstonia solanacearum by Regulating CaPR1 and CaPR1L Expression[J]. Acta Horticulturae Sinica, 2026, 53(3): 831-844.

图/表 10

表1 本研究中用于VIGS、EMSA、DLR及RT-qPCR的引物序列

Table 1 Primer sequences used for VIGS，EMSA，DLR，and RT-qPCR in this study

用途Application	引物名称Primer name	正向引物（5°-3°）Forward	反向引物（5°-3°）Reverse
病毒诱导基因沉默 VIGS	PYL-279-wrky271	ggggacaagtttgtacaaaaaagcaggcttcCGACTTCTGATATTCCGGTT	ggggaccactttgtacaagaaagctgggtcCCCTTGAACATTCCGGTAACT
病毒诱导基因沉默 VIGS	PYL-279-wrky272	ggggacaagtttgtacaaaaaagcaggcttcTATTTGGCCGTGGAATGATGG	ggggaccactttgtacaagaaagctgggtcTTATTTTACTATACTACAAAAC
凝胶阻滞实验 EMSA	CaWRKY27-MBP	aaggatttcagaattcATGGAAGGAAGATTCAACAA	gcaggtcgactctgacttaGCCTGTGGTCCCACACCAC
	CaPR1-Cy5-EMSA （WT）	AGGAGGCTGGCTGCGCT TGACTATGTATATATATTGGCATTA	TAATGCCAATATATATACATA GTCAAGCGCAGCCAGCCTCCT
	CaPR1-Cy5-EMSA （mut）	AGGAGGCTGGCTGCGCT T t A tTATGTATATATATTGGCATTA	TAATGCCAATATATATACATA a T a AAGCGCAGCCAGCCTCCT
	CaPR1L-Cy5-EMSA （WT）	CAAAATTTGAAAAC GTCAATAGATAGTAACTCTTCTAAAG	CTTTAGAAGAGTTACTATCTAT TGACGTTTTCAAATTTTG
	CaPR1L-Cy5-EMSA （mut）	CAAAATTTGAAAAC aTaAATAGATAGTAACTCTTCTAAAG	CTTTAGAAGAGTTACTATCTAT TtAtGTTTTCAAATTTTG
双荧光素报告实验 DLR	CaWRKY27-p62SK	cgctctagaactagtggatccATGGAAGGAAGATTCAACAA	gtcgacggtatcgataagcttTTAGCCTGTGGTCCCACACCAC
	CaPR1p-0800	gtcgacggtatcgataagcttCAACCAAAAGAGTTTTGAGCTTTCT	cgctctagaactagtggatccTTTGGGTTTTGGTGAGAATTAAGG
	CaPR1Lp-0800	gtcgacggtatcgataagcttCCCCGTGGAAATTTCGCT	cgctctagaactagtggatccTTCGGGTTTTGATGAGAACAAGG
实时荧光定量PCR RT-qPCR	qCaActin	AGGGATGGGTCAAAAGGATGC	GAGACAACACCGCCTGAATAGC
	qCaWRKY27	CTGAGCAAGATGATTCCGAGAA	ATTGGCACTGACACCACTCT
	qCaPR1	CGTGAAGATGTGGTTCGATG	AGGCAGGTTGTTCTTCCAGA
	qCaPR1L	CGTGAAGATGTGGGTCAATG	CCATACGGACGTTGTCCTCT
	qCaPR5	CTCTGAAGCAGCAACATTCG	GTCCAAAAGATTGGCATTGG

图1 辣椒、番茄及拟南芥WRKYⅡe亚家族成员的系统进化树 A：辣椒（Ca）、番茄（Sl）和拟南芥（At）WRKYⅡe亚家族成员系统进化树；B：辣椒（Ca）和番茄（Sl）WRKYⅡe亚家族成员系统进化树。采用极大似然法构建进化树

Fig. 1 Phylogenetic analysis of WRKYⅡe subfamily members from Arabidopsis，tomato，and pepper A：Phylogenetic analysis of WRKYⅡe subfamily members in pepper（Ca），tomato（Sl），and Arabidopsis（At）；B：Phylogenetic analysis of WRKYⅡe subfamily members in pepper（Ca）and tomato（Sl）. The tree was constructed using the maximum likelihood method

图2 辣椒CaWRKY27与番茄SlWRKY79、拟南芥AtWRKY65的WRKY结构域多序列比对红框突出显示的氨基酸代表在WRKYⅡe亚家族成员中发现的保守残基。At：拟南芥；Ca：辣椒；Sl：番茄

Fig. 2 Multiple sequence comparison of WRKY domains in pepper CaWRKY27，tomato SlWRKY79，and Arabidopsis AtWRKY65 The amino acids highlighted in the red box represent the conserved residues found in WRKYⅡe subfamily members. At：Arabidopsis thaliana；Ca：Capsicum annuum；Sl：Solanum lycopersicum

图3 辣椒CaWRKY27启动子区域主要的顺式作用元件分布

Fig. 3 The distribution of main cis-elements in the promoter region of the pepper CaWRKY27

表2 辣椒CaWRKY27启动子区域鉴定的主要顺式作用元件

Table 2 Identified main cis-elements in the promoter region of the pepper CaWRKY27

元件 Element	序列 Sequence	位置/bp Location	数量 Number	位点功能 Function of site
MBSI	TTTTTACGGTTA	-556	1	参与类黄酮生物合成基因调控的MYB结合位点 MYB binding site involved in flavonoid biosynthetic genes regulation
ATC-motif	TGCTATCCA	-1 646	1	参与光响应的保守DNA基序的一部分 Part of a conserved DNA module involved in light responsiveness
ATCT-motif	AATCTAATCC	-1 757	1	参与光响应的保守DNA基序的一部分 Part of a conserved DNA module involved in light responsiveness
O₂-site	GATGATGTGG	-1 860	1	参与玉米醇溶蛋白代谢调控的顺式作用调节元件 cis-Acting regulatory element involved in zein metabolism regulation
ABRE	ACGTG	-1 251/-218	2	参与脱落酸响应的顺式作用元件 cis-Acting element involved in the abscisic acid responsiveness
TCA-element	CCATCTTTTT	-406	1	参与水杨酸响应的顺式作用元件 cis-Acting element involved in salicylic acid responsiveness
GATA- motif	AAGGATAAGG	-1 127	1	光响应元件的一部分Part of a light responsive element
TC-rich repeats	GTTTTCTTAC	-1 161	1	参与防御和胁迫响应的顺式作用元件 cis-Acting element involved in defense and stress responsiveness
Box 4	ATTAAT	-1 612/-1 294	2	参与光响应的保守DNA模块的一部分 Part of a conserved DNA module involved in light responsiveness
AuxRR-core	GGTCCAT	-1 475	1	参与生长素响应的顺式作用调控元件 cis-Acting regulatory element involved in auxin responsiveness
I-box	AGATAAGG	-184	1	光响应元件的一部分Part of a light responsive element
G-Box	CACGTT	-1 251/-217	2	参与光响应的顺式作用调控元件 cis-Acting regulatory element involved in light responsiveness
ARE	AAACCA	-1 592	1	厌氧诱导所必需的顺式作用元件 cis-Acting regulatory element essential for the anaerobic induction
MBS	CAACTG	-1 987/-1 666	2	参与干旱诱导的MYB结合位点 MYB binding site involved in drought inducibility
ERE	ATTTCATA	-125	1	参与光响应的顺式作用元件 cis-Acting regulatory element involved in light responsiveness

表2 辣椒CaWRKY27启动子区域鉴定的主要顺式作用元件

Table 2 Identified main cis-elements in the promoter region of the pepper CaWRKY27

元件 Element	序列 Sequence	位置/bp Location	数量 Number	位点功能 Function of site
MBSI	TTTTTACGGTTA	-556	1	参与类黄酮生物合成基因调控的MYB结合位点 MYB binding site involved in flavonoid biosynthetic genes regulation
ATC-motif	TGCTATCCA	-1 646	1	参与光响应的保守DNA基序的一部分 Part of a conserved DNA module involved in light responsiveness
ATCT-motif	AATCTAATCC	-1 757	1	参与光响应的保守DNA基序的一部分 Part of a conserved DNA module involved in light responsiveness
O₂-site	GATGATGTGG	-1 860	1	参与玉米醇溶蛋白代谢调控的顺式作用调节元件 cis-Acting regulatory element involved in zein metabolism regulation
ABRE	ACGTG	-1 251/-218	2	参与脱落酸响应的顺式作用元件 cis-Acting element involved in the abscisic acid responsiveness
TCA-element	CCATCTTTTT	-406	1	参与水杨酸响应的顺式作用元件 cis-Acting element involved in salicylic acid responsiveness
GATA- motif	AAGGATAAGG	-1 127	1	光响应元件的一部分Part of a light responsive element
TC-rich repeats	GTTTTCTTAC	-1 161	1	参与防御和胁迫响应的顺式作用元件 cis-Acting element involved in defense and stress responsiveness
Box 4	ATTAAT	-1 612/-1 294	2	参与光响应的保守DNA模块的一部分 Part of a conserved DNA module involved in light responsiveness
AuxRR-core	GGTCCAT	-1 475	1	参与生长素响应的顺式作用调控元件 cis-Acting regulatory element involved in auxin responsiveness
I-box	AGATAAGG	-184	1	光响应元件的一部分Part of a light responsive element
G-Box	CACGTT	-1 251/-217	2	参与光响应的顺式作用调控元件 cis-Acting regulatory element involved in light responsiveness
ARE	AAACCA	-1 592	1	厌氧诱导所必需的顺式作用元件 cis-Acting regulatory element essential for the anaerobic induction
MBS	CAACTG	-1 987/-1 666	2	参与干旱诱导的MYB结合位点 MYB binding site involved in drought inducibility
ERE	ATTTCATA	-125	1	参与光响应的顺式作用元件 cis-Acting regulatory element involved in light responsiveness

图4 辣椒CaWRKY27沉默与对照辣椒植株中SA途径防御基因CaPR1、CaPR1L和CaPR5的表达模式

Fig. 4 The expression pattern of the SA signaling pathway-related defence genes CaPR1，CaPR1L，and CaPR5 in CaWRKY27-silenced and control pepper plants ** P < 0.01

图5 辣椒CaWRKY27与靶基因CaPR1和CaPR1L启动子W-box元件的凝胶阻滞实验 A：EMSA实验中使用的寡核苷酸探针的示意图；B：EMSA检测CaWRKY27与CaPR1和CaPR1L启动子的体外结合。分别以不添加任何蛋白和只添加MBP蛋白作为对照，实验组均添加MBP-CaWRKY27蛋白。下划线标记部分表示顺式作用元件W-Box。“+”表示添加探针，“-”表示不添加探针

Fig. 5 EMSA for the binding of the pepper CaWRKY27 to the promoters of target genes CaPR1 and CaPR1L A：Schematic diagram of the oligonucleotide probes used in the EMSA experiments；B：EMSA detection of binding of CaWRKY27 to CaPR1 and CaPR1L promoters in vitro. MBP protein and no protein were used as control，respectively，and all experimental groups were added with MBP-CaWRKY27 protein. The underlined nucleotide sequences represents the cis-acting element W-box. The symbols“+”and“-”represent presence or absence of the probe

图6 双荧光素报告实验检测CaWRKY27对靶基因CaPR1和CaPR1L启动子活性的影响 A：效应载体和报告载体示意图；B：CaPR1和CaPR1L启动子的相对活性

Fig. 6 Dual-luciferase reporter assay to detect for the effect of CaWRKY27 on the promoter activity of target genes CaPR1 and CaPR1L A：Schematic diagram of the reporter vector and effector vector；B：Relative activity of the CaPR1 and CaPR1L promoters. ** P < 0.01

图7 瞬间表达实验分析CaWRKY27对靶基因CaPR1和CaPR1L启动子驱动LUC报告基因表达的影响

Fig. 7 Transient expression assay to analyze the effect of CaWRKY27 on the expression of LUC reporter gene driven by the promoters of target genes CaPR1 and CaPR1L

图8 CaWRKY27调控辣椒抗青枯病的工作模型 SA诱导了转录因子CaWRKY27的表达，随后CaWRKY27通过直接激活SA信号途径防御基因CaPR1 和CaPR1L的表达，从而增强了辣椒对青枯病的抗性

Fig. 8 Proposed working model of the CaWRKY27 in regulating pepper resistance to bacterial wilt SA induces the expression of the transcription factor CaWRKY27，which subsequently directly activates the expression of SA signaling pathway-related defence genes CaPR1 and CaPR1L，thereby enhancing pepper resistance to bacterial wilt

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