转录因子NbMYB1R1通过促进活性氧积累抑制病毒侵染

doi:10.3864/j.issn.0578-1752.2024.08.006

中国农业科学 ›› 2024, Vol. 57 ›› Issue (8): 1490-1505.doi: 10.3864/j.issn.0578-1752.2024.08.006

转录因子NbMYB1R1通过促进活性氧积累抑制病毒侵染

姜兴林¹(), 于连伟¹(), 付涵¹, 艾妞¹, 崔荧钧⁵, 李好海⁶, 夏子豪⁷, 袁虹霞¹, 李洪连¹^,³^,⁴, 杨雪¹^,²(), 施艳¹()

¹ 河南农业大学植物保护学院，郑州 450002
² 河南农业大学作物学博士后流动站，郑州 450002
³ 河南省粮食作物协同创新中心，郑州 450002
⁴ 小麦玉米作物学国家重点实验室，郑州 450002
⁵ 河南省植物保护新技术推广协会，郑州 450002
⁶ 河南省植物保护检疫站，郑州 450002
⁷ 沈阳农业大学植物保护学院，沈阳 110866

收稿日期:2023-12-06 接受日期:2024-02-04 出版日期:2024-04-16 发布日期:2024-04-24
通信作者:
杨雪，E-mail：yangxuepphappy@126.com。
施艳，E-mail：shiyan00925@126.com
联系方式: 姜兴林，E-mail：1442295312@qq.com。于连伟，E-mail：ylwnet972@163.com。姜兴林和于连伟为同等贡献作者。
基金资助:
国家自然科学基金(3210170372); 河南农业大学科技创新项目(KJCX2021A13)

The Transcription Factor NbMYB1R1 Inhibits Viral Infection by Promoting ROS Accumulation

JIANG XingLin¹(), YU LianWei¹(), FU Han¹, AI Niu¹, CUI YingJun⁵, LI HaoHai⁶, XIA ZiHao⁷, YUAN HongXia¹, LI HongLian¹^,³^,⁴, YANG Xue¹^,²(), SHI Yan¹()

¹ College of Plant Protection, Henan Agricultural University, Zhengzhou 450002
² Crop Science Postdoctoral Programme of Henan Agricultural University, Zhengzhou 450002
³ Collaborative Innovation Centre of Henan Grain Crops, Zhengzhou 450002
⁴ State Key Laboratory of Wheat and Maize Crop Science, Zhengzhou 450002
⁵ Henan Association for the Promotion of New Plant Protection Techniques, Zhengzhou 450002
⁶ Henan Plant Protection and Quarantine Station, Zhengzhou 450002
⁷ College of Plant Protection, Shenyang Agricultural University, Shenyang 110866

Received:2023-12-06 Accepted:2024-02-04 Published:2024-04-16 Online:2024-04-24

摘要/Abstract

摘要：

【背景】黄瓜绿斑驳花叶病毒（cucumber green mottle mosaic virus，CGMMV）是我国重要的检疫性植物病毒，严重降低了世界范围内蔬菜以及瓜类的产量。MYB蛋白家族庞大，功能多样，存在于所有真核生物中。大多数MYB作为转录因子控制植物的发育和代谢，并对植物应对生物和非生物胁迫反应起重要的调控作用。前期研究显示CGMMV侵染后可以显著上调寄主转录因子基因NbMYB1R1的表达。【目的】明确NbMYB1R1参与CGMMV侵染的机制，为CGMMV病害防控提供理论依据。【方法】运用MEGA 7.0构建系统进化树，对NbMYB1R1的氨基酸序列进行系统进化分析；通过构建NbMYB1R1的荧光表达载体，转化GV3101农杆菌后浸润本氏烟叶片，激光共聚焦显微镜观察其亚细胞定位；利用qRT-PCR技术分析NbMYB1R1在CGMMV侵染不同时期的转录水平及NbMYB1R1沉默烟草植株中活性氧（reactive oxygen species，ROS）相关基因的转录变化；通过沉默NbMYB1R1及下游调控基因NbAOX1a和NbAOX1b，分析NbMYB1R1及下游调控基因NbAOX1a和NbAOX1b在CGMMV侵染过程中的作用；瞬时过表达NbMYB1R1和NbMYB1R1关键氨基酸突变体，分析NbMYB1R1对CGMMV侵染的影响；使用台盼蓝染色以及DAB染色观察瞬时过表达NbMYB1R1造成的细胞死亡是否与程序性细胞死亡（programmed cell death，PCD）以及ROS的积累有关；运用酵母双杂交技术验证NbMYB1R1是否与CGMMV相关蛋白互作。【结果】系统进化树分析表明，NbMYB1R1属于1R MYB大类并与多种烟草的MYB转录因子同源性极高；亚细胞定位结果显示NbMYB1R1定位于细胞核；在CGMMV侵染的烟草植株中，NbMYB1R1的转录水平对比健康植株有明显变化，在CGMMV侵染8、12 d时NbMYB1R1的转录水平显著上调；在沉默内源基因NbMYB1R1的植株上接种CGMMV，3 d后NbMYB1R1沉默植株系统叶出现斑驳、卷曲症状，而对照植株在3.5 d时才出现症状；同时CGMMV CP mRNA水平和蛋白水平检测结果也表明沉默NbMYB1R1可以有效促进CGMMV的积累；在本氏烟叶片瞬时过表达NbMYB1R1及其突变体3 d时检测CGMMV蛋白水平表达量，结果显示过表达NbMYB1R1可以有效抑制CGMMV的侵染，DNA结合结构域缺失后会减轻NbMYB1R1对CGMMV的抑制；台盼蓝和DAB染色结果表明，在瞬时过表达NbMYB1R1蛋白后导致ROS积累并引起细胞死亡；在沉默内源基因NbMYB1R1的植株叶片上检测ROS相关基因的转录水平，发现交替氧化酶基因AOX1a、AOX1b转录水平显著上调；在沉默内源基因NbAOX1a和NbAOX1b的植株上接种CGMMV，4 d后NbAOX1a和NbAOX1b沉默植株系统叶出现斑驳、卷曲症状，而对照植株在3.5 d时就出现症状；同时CGMMV CP mRNA水平和蛋白水平检测结果也表明沉默NbAOX1a和NbAOX1b可以有效抑制CGMMV的积累；酵母双杂交结果显示NbMYB1R1不与CGMMV编码蛋白直接相互作用。【结论】随着CGMMV侵染，防御相关基因NbMYB1R1表达上调，从而抑制下游基因AOX1a、AOX1b的表达并激活细胞内产生ROS抑制病毒侵染，但NbMYB1R1不是通过与CGMMV病毒蛋白直接互作而产生此作用。由此可见，NbMYB1R1在CGMMV侵染过程中发挥了重要作用。

关键词: 黄瓜绿斑驳花叶病毒, NbMYB1R1, 转录因子, 致病机制, 活性氧

Abstract:

【Background】Cucumber green mottle mosaic virus (CGMMV) is an important quarantine plant virus in China, which has seriously reduced the production of vegetables and melons worldwide. The MYB protein family is large, multifunctional and present in all eukaryotes. Most MYB proteins act as transcription factors that control development, and metabolism in plants, and regulate biotic and abiotic stress responses. Previous studies have shown that during CGMMV infection, the expression of transcription factor gene NbMYB1R1 was significantly up-regulated. 【Objective】The objective of this study is to clarify the mechanism of NbMYB1R1 involved in CGMMV infection, and to provide a theoretical basis for controlling CGMMV infection. 【Method】MEGA 7.0 was used to construct a phylogenetic tree to analyze the amino acid sequence of NbMYB1R1 protein. The expression vector NbMYB1R1-GFP was constructed, transformed into Agrobacterium GV3101 and infiltrated the tobacco leaves to observe the subcellular localization of NbMYB1R1 by confocal microscopy. The transcriptional levels of NbMYB1R1 at different stages of CGMMV infection and ROS related genes in silenced NbMYB1R1 plants were analyzed using qRT-PCR technology. TRV-mediated gene silencing (VIGS) was utilized to analyze the function of NbMYB1R1, NbAOX1a, and NbAOX1b during CGMMV infection. Transient overexpression of NbMYB1R1 and NbMYB1R1 mutant was conducted to analyze the effect of NbMYB1R1 on CGMMV infection. Trypan blue staining and DAB staining were used to observe whether the cell death caused by the transient overexpression of NbMYB1R1 was related to the programmed cell death (PCD) and the accumulation of ROS. Yeast two-hybrid system was used to verify whether NbMYB1R1 interacted with CGMMV related proteins. 【Result】Phylogenetic tree analysis showed that NbMYB1R1 belonged to the 1R MYB category and had high homology with MYB transcription factors in a variety of tobaccos. The results of subcellular localization showed that NbMYB1R1 was localized in the nucleus. In CGMMV-infected tobacco plants, the transcript level of NbMYB1R1 was significantly changed compared with healthy plants, which was significantly up-regulated at 8 and 12 d of CGMMV infection. CGMMV was inoculated into TRV:NbMYB1R1 and TRV:00 plants. The NbMYB1R1-silenced plants showed the mottled and curled symptoms at 3 dpi, while the control plant appeared the symptoms at 3.5 dpi. Silencing NbMYB1R1 could effectively promote the accumulation of CGMMV at mRNA and protein levels. The CGMMV accumulation in NbMYB1R1 and NbMYB1R1 mutant transiently overexpression leaves was detected, and the results showed that NbMYB1R1 overexpression could effectively inhibit CGMMV infection and DNA binding domain deletion mutant reduced the inhibition of CGMMV by NbMYB1R1. The results of trypan blue and DAB staining showed that NbMYB1R1 overexpression could induce the ROS accumulation and cell death. The transcription level of ROS-related genes in TRV:NbMYB1R1 and TRV:00 plant was also detected, and the results showed that silencing NbMYB1R1 could specifically up-regulate the transcription of AOX1a and AOX1b. After CGMMV inoculation on silencing endogenous genes NbAOX1a and NbAOX1b, the systemic leaves of silenced NbAOX1a and NbAOX1b plants showed mottled and curled symptoms at 4 dpi, while the control plants appeared symptoms at 3.5 d. Meanwhile, the results of CGMMV CP mRNA and protein levels also indicated that silencing NbAOX1a and NbAOX1b could effectively inhibit the accumulation of CGMMV. The yeast two-hybrid results showed that NbMYB1R1 did not directly interact with the CGMMV proteins. 【Conclusion】During the CGMMV infection, the defense-related gene NbMYB1R1 is up-regulated. It speculates that the upregulation of NbMYB1R1 inhibits the transcription of the downstream genes AOX1a and AOX1b and activates the production of ROS in cells, thereby inhibiting viral infection. However, NbMYB1R1 does not produce this effect through a direct interaction with the CGMMV viral protein. NbMYB1R1 plays an important role in CGMMV infection.

Key words: cucumber green mottle mosaic virus (CGMMV), NbMYB1R1, transcription factor, pathogenic mechanism, reactive oxygen species (ROS)

姜兴林, 于连伟, 付涵, 艾妞, 崔荧钧, 李好海, 夏子豪, 袁虹霞, 李洪连, 杨雪, 施艳. 转录因子NbMYB1R1通过促进活性氧积累抑制病毒侵染[J]. 中国农业科学, 2024, 57(8): 1490-1505.

JIANG XingLin, YU LianWei, FU Han, AI Niu, CUI YingJun, LI HaoHai, XIA ZiHao, YUAN HongXia, LI HongLian, YANG Xue, SHI Yan. The Transcription Factor NbMYB1R1 Inhibits Viral Infection by Promoting ROS Accumulation[J]. Scientia Agricultura Sinica, 2024, 57(8): 1490-1505.

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图/表 11

表1

本研究所用引物"

用途Use	引物名称Primer name	引物序列Primer sequence (5′-3′)
酵母双杂交系统 Yeast two-hybrid	pGADT7- NbMYB1R1-F	ATATGGCCATGGAGGCCAGTGAATTCATGTCTAACGAATGCGGAAACAAAGA
	pGADT7- NbMYB1R1-R	ATCTGCAGCTCGAGCTCGATGGATCCAGCCACACTAATTATGCTATCCCC
	pGBKT7-CP-F	TGCATATGGCCATGGAGGCCGAATTCATGGCTTACAATCCGATCACACCTA
	pGBKT7-CP-R	TGCGGCCGCTGCAGGTCGACGGATCCAGCTTTCGAGGTGGTAGCC
	pGBKT7-MP-F	TGCATATGGCCATGGAGGCCGAATTCATGTCTCTAAGTAAGGTGTCAGTCG
	pGBKT7-MP-R	TGCGGCCGCTGCAGGTCGACGGATCCGGTGTGATCGGATTGTAAGCC
	pGBKT7-129K-F	TGCATATGGCCATGGAGGCCGAATTCATGGCAAACATTAATGAACAAATCA
	pGBKT7-129K-R	TGCGGCCGCTGCAGGTCGACGGATCCTTTGGTAGGCACAGTGGTAGC
	pGBKT7-MET-F	TGCATATGGCCATGGAGGCCGAATTCATGGCAAACATTAATGAACAAATCA
	pGBKT7-MET-R	TGCGGCCGCTGCAGGTCGACGGATCCCTCGATCTGTACCTTCCTAACCTTCA
	pGBKT7-HEL-F	TGCATATGGCCATGGAGGCCGAATTCACATTAGTTGACGGAGTGCC
	pGBKT7-HEL-R	TGCGGCCGCTGCAGGTCGACGGATCCTTTGGTAGGCACAGTGGTAGC
	pGBKT7-P2-F	TGCATATGGCCATGGAGGCCGAATTCCAATTAATGCAGAACTCGCTGTATG
	pGBKT7-P2-R	TGCGGCCGCTGCAGGTCGACGGATCCCTTAGAGACATCTATGTAAAGACTAC
瞬时过表达 Over-expression	NbMYB1R1-GFP-F	ACGAGCTGTACAAGGGTACCATGTCTAACGAATGCGGAAACAAAGA
	NbMYB1R1-GFP-R	CGGACTCTAGTTCATCTAGAAGCCACACTAATTATGCTATCCCC
	NbMYB1R1^121-127-GFP-F	CCTACTCAGGTGGCCCTCCGCCGAAATAACATCAA
	NbMYB1R1^121-127-GFP-R	GTTATTTCGGCGGAGGGCCACCTGAGTAGGGGTC
基因沉默 Virus induced gene silencing (VIGS)	NbMYB1R1 VIGS-F	AGTGGTCTCTGTCCAGTCCTCAAGACAAGGACCCCTACTC
	NbMYB1R1 VIGS-R	GGTCTCAGCAGACCACAAGTGGTATTGGCCTAATGGGCT
	NbAOX1a/b VIGS-F	AGTGGTCTCTGTCCAGTCCT GTAGGAGGAATGTTGTTGCACT
	NbAOX1a/b VIGS-R	GGTCTCAGCAGACCACAAGT ATTACCCTTGTCTAATTCCTTGAGG
实时荧光定量PCR Quantitative real-time PCR	NbUBC-qPCR-F	TTTCGGTCCTGATGATACTCCC
	NbUBC-qPCR-R	CACAGAGCAAAGACTGGATTGA
	NbMYB1R1-qPCR-F	GGGTTCATGCTCTTTGGTGT
	NbMYB1R1-qPCR-R	ACGGGTCCTAGCAGAAGGAT
	NbAOX1a-qPCR-F	TTGAGAACGTTCCTGCTCCT
	NbAOX1a-qPCR-R	TGGAGAGTCCCTTGAGCTGT
	NbAOX1b-qPCR-F	TTGAGAACGTTCCTGCTCCT
	NbAOX1b-qPCR-R	GGTGCTGGAGAGTCCTTGAG
	NbGST-qPCR-F	TGAAGGAAAGCGAAGCACAAT
	NbGST-qPCR-R	ACGACGGCGCGAATCAAACA
	NbSOD-qPCR-F	GCCGTCCTTAGCAGCAGTGAA
	NbSOD-qPCR-R	CCGGGTTTTAGGCCAGAGACAT
	NbAPX1-qPCR-F	GGAGTGGTTGCTGTTGAAGTC
	NbAPX1-qPCR-R	GGAGAGCCTTGTCTGATGG
	NbCAT3-qPCR-F	TGCGCATCACAATAATCACCAT
	NbCAT3-qPCR-R	TGTCGCGCTTTCCTGTCAA
	NbGPX2-qPCR-F	TTGTTTTGCCACTACCTTGTTCAG
	NbGPX2-qPCR-R	TTCATTTGGGGGTGTCAGATTAG
	CP-qPCR-F	ACAAGGTACCGCTTTCCAGA
	CP-qPCR-R	TACGACAGACGAGGGTAACG

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转录因子NbMYB1R1通过促进活性氧积累抑制病毒侵染

The Transcription Factor NbMYB1R1 Inhibits Viral Infection by Promoting ROS Accumulation

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