旱柳SmERF B3-45的克隆及耐盐功能研究

doi:10.13560/j.cnki.biotech.bull.1985.2024-0385

摘要/Abstract

摘要：

【目的】验证SmERF B3-45是否在植物响应盐胁迫中起着正向调控的作用，为揭示AP2/ERF转录因子在调控旱柳耐盐性中的作用奠定基础。【方法】分析旱柳AP2/ERF超家族中SmERF B3-45的启动子区顺式作用元件，利用特异性引物克隆得到SmERF B3-45的CDS全长序列，对其进行生物信息学和亚细胞定位分析，并通过过表达载体的构建转化拟南芥突变体ERF-OE1、ERF-OE2和进行病毒诱导的基因沉默（VIGS）阐明其功能。【结果】顺式作用元件分析表明，SmERF B3-45可能参与逆境胁迫响应表达调控途径。RT-qPCR结果显示，NaCl处理可诱导SmERF B3-45的表达，且该基因在旱柳的不同组织中广泛表达。亚细胞定位显示，SmERF B3-45蛋白定位于细胞核。转基因拟南芥中，SmERF B3-45的表达量大幅提高，在盐胁迫条件下，与野生型相比，过表达SmERF B3-45拟南芥的根长显著增加，总蛋白含量、Na⁺含量、MDA含量和Na⁺/K⁺显著降低，CAT含量和K⁺含量显著升高。基因沉默植株显著下调了SmERF B3-45的表达水平，与对照相比，基因沉默植株的总蛋白含量显著降低，而MDA和脯氨酸含量却显著高于阴性对照植株，并且沉默植株出现了叶片萎蔫，表明SmERF B3-45的沉默降低了旱柳的耐盐性。【结论】SmERF B3-45是植物响应盐胁迫的正向调控转录因子。

关键词: 旱柳, 基因克隆, 盐胁迫, ERF转录因子, 转基因, 病毒诱导的基因沉默（VIGS）

Abstract:

【Objective】To validate whether SmERF B3-45 plays a positive regulatory role in plant response to salt stress may lay the foundation for revealing the role of AP2/ERF transcription factors in regulating the salt tolerance of Salix matsudana.【Method】The cis-acting elements in the promoter region of SmERF B3-45 from the AP2/ERF superfamily of Populus euphratica were analyzed. The full-length CDS sequence of SmERF B3-45 was cloned using specific primers, and bioinformatics and subcellular localization analysis were conducted. The function was elucidated by constructing overexpression vectors and transforming Arabidopsis thaliana mutants ERF-OE1 and ERF-OE2, and by using virus-induced gene silencing（VIGS）.【Result】Cis-acting element analysis suggested that SmERF B3-45 may be involved in the expression regulation pathways responding to stress. RT-qPCR results showed that the expression of SmERF B3-45 was induced by NaCl treatment and was widely expressed in different tissues of Populus euphratica. Subcellular localization indicated that the SmERF B3-45 protein was localized in the nucleus. In transgenic Arabidopsis, the expression of SmERF B3-45 significantly increased. Under salt stress, compared with the wild type, the root length of overexpressing SmERF B3-45 Arabidopsis significantly increased, while the total protein content, Na⁺ content, MDA content, and Na⁺/K⁺ ratio significantly decreased, and the CAT content and K⁺content significantly increased. Gene-silenced plants showed a significant downregulation of SmERF B3-45 expressions. Compared with the control, the total protein content of the gene-silenced plants significantly reduced, while MDA and proline content were significantly higher than that of the negative control plants. Additionally, the silenced plants demonstrated wilting leaves, indicating that the silencing of SmERF B3-45 reduced the tolerance of Salix matsudana to salt. 【Conclusion】SmERF B3-45 is confirmed as a positive regulatory transcription factor in the plant response to salt stress.

Key words: Salix matsudana, gene cloning, salt stress, ERF transformation factor, genetic transformation, virus-induced gene silencing（VIGS）

华炫, 田博雯, 周欣彤, 江梓涵, 王诗琦, 黄倩慧, 张健, 陈艳红. 旱柳SmERF B3-45的克隆及耐盐功能研究[J]. 生物技术通报, 2024, 40(12): 124-135.

HUA Xuan, TIAN Bo-wen, ZHOU Xin-tong, JIANG Zi-han, WANG Shi-qi, HUANG Qian-hui, ZHANG Jian, CHEN Yan-hong. Cloning SmERF B3-45 from Salix matsudana and Functional Analysis on Its Tolerance to Salt[J]. Biotechnology Bulletin, 2024, 40(12): 124-135.

图/表 11

图1 AP2/ERF家族分类红星表示Soloist 亚家族成员含有保守程度较低的AP2结构域

Fig. 1 AP2/ERF family classification The red star indicates that members of the Soloist subfamily contain AP2 domains with a lower degree of conservatism

表1 本研究所用引物信息

Table 1 Information of primers used in this study

引物名称 Primer name	引物序列 Primer sequence（5'-3'）
SmERF B3-45F	ATGTCGCAAGGAGGGAACA
SmERF B3-45R	TCATTTTCTTCTCTTGGGC
pWM101-SmERF B3-45F	TCGAGCTTTCGCGAGCTCGGTACCATGTCGCAAGGAGGGAACA
pWM101-SmERF B3-45R	GCATGCCTGCAGGTCGACTCTAGATCATTTTCTTCTCTTGGGC
P2300-SmERF B3-45F	GACGAGCTGTACAAGGGATCCATGTCGCAAGGAGGGAACA
P2300-SmERF B3-45R	CTGCAGGTCGACTCTAGATCATCATTTTCTTCTCTTGGGC
qPCR-SmERF B3-45F	AGCAAGGATGTGGCTTGGAA
qPCR- SmERF B3-45R	CTTCTCTTGGGCGAGCCATC
TRV2- SmERF B3-45F	TAAGGTTACCGAATTCTCGCAAGGAGGGAACAACAG
TRV2- SmERF B3-45R	CGAGACGCGTGAGCTCTCTTACACGCCACTTCCACC

图2 旱柳SmERF B3-45启动子顺式作用元件

Fig. 2 Cis-acting elements of SmERF B3-45 promoter in S. matsudana Koidz

表2 SmERF B3-45启动子区顺式作用元件预测结果

Table 2 Predicted results of cis-acting elements in the SmERF B3-45 promoter region

种类Type	功能 Function	元件 Element	数目 Amount
光响应元件Light responsive elements	光响应Light responsiveness	G-box	5
		TCT-motif	2
		Box 4	4
		ATCT-motif	1
		AT1-motif	1
		I-box	1
激素响应元件Phytohormone responsive elements	脱落酸响应Abscisic acid responsiveness	ABRE	6
激素响应元件Phytohormone responsive elements	赤霉素响应Gibberellin-responsiveness	TATC-box	1
逆境响应元件Stress responsive elements	抗氧Antioxidant	O2-site	1
逆境响应元件Stress responsive elements	干旱、盐和低温响应 Drought, salt and low temperature responsive	MYB	1

图3 SmERF B3-45的克隆和植物表达载体的构建 A：SmERF B3-45的PCR扩增产物的电泳检测；B：过表达载体pWM101-SmERF B3-45单酶切（BamH I）验证；C：VIGS中pYL1561- SmERF B3-45载体双酶切（EcoR I+Sal I）验证；D：亚细胞定位p2300-SmERF B3-45载体双酶切（Kpn I+Sal I）验证

Fig. 3 Cloning of SmERF B3-45 and construction of plant expression vector construction A: PCR amplification product detection of SmERF B3-45. B: Overexpression vector pWM101-SmERF B3-45 single enzyme digestion（BamH I）verification. C: VIGS vector pYL1561-SmERF B3-45 double enzyme digestion（EcoR I+Sal I）verification. D: Subcellular localization vector p2300-SmERF B3-45 double enzyme digestion（Kpn I+Sal I）verification

图4 SmERF B3-45及其同源物的系统发生树构建和蛋白质比对 A：系统进化树；B：同源蛋白比对。Sabra14G0034100：白柳；Potri.014G047000、Potri.003G150700、Potri.003G150800：毛果杨； Gohir.D08G067700：棉花；BraA04t18813Z、BraA05t19475Z：白菜型油菜；Manes.05G054400：木薯；AT2G44840_ERF13、AT2G31230_ERF15、AT4G17490_ERF6：拟南芥。SmERF B3-45蛋白与其直系蛋白质中有一个AP2结构域，已用红色线标记

Fig. 4 Phylogenetic tree construction and protein alignment on SmERF B3-45 protein and its homologs A: Phylogenetic tree. B: Homologous protein alignment. Sabra14G0034100: S. alba; Potri.014G047000, Potri.003G150700, Potri.003G150800: Populus alba; Gohir.D08G067700: G. herbaceum; BraA04t18813Z, BraA05t19475Z: B. rapa; Manes.05G054400: M. esculenta; AT2G44840_ERF13, AT2G31230_ERF15, AT4G17490_ERF6: Arabidopsis thaliana. The SmERF B3-45 protein shares an AP2 domain with its orthologous proteins, which has been marked with a red line

图5 SmERF B3-45的表达谱分析 A：SmERF B3-45在旱柳不同组织中的表达；B：经200 mmol/L NaCl处理0, 4, 8和12 h后SmERF B3-45的表达。不同小写字母表示显著差异（P<0.05），下同

Fig. 5 Expression pattern analysis of SmERF B3-45 A: Expressions of SmERF B3-45 in different tissues of Salix matsudana. B: Expressions of SmERF B3-45 after treatment with 200 mmol/L NaCl for 0, 4, 8 and 12 h. Different small letters indicate significant differences（P<0.05）. The same below

图6 SmERF B3-45蛋白的亚细胞定位分析 A：激光共聚焦显微镜明场，显示叶片细胞的气孔结构；B：GFP信号通道显示SmERF B3-45蛋白的定位信号；C：mCherry信号通道显示组蛋白H2B核定位信号；D：为A、B、C通道叠加，显示SmERF B3-45蛋白的定位信号和组蛋白H2B核定位信号共定位

Fig. 6 Subcellular localization analysis of SmERF B3-45 protein A: Laser confocal microscopy to display the stomatal structure of leaf cells.B: GFP signal channel displays the localization signal of SmERF B3-45 protein. C: mCherry signal channel displays histone H2B nuclear localization signals.D: Overlay of channels of A, B, and C, display co-localization of SmERF B3-45 protein localization signal and histone H2B nuclear localization signal

图7 SmERF B3-45拟南芥过表达株系的表型分析 A：0和100 mmol/L NaCl处理7 d后各株系的生长情况；B：0和100 mmol/L NaCl处理7 d后各株系根长的统计

Fig. 7 Phenotypic analysis of SmERF B3-45 overexpressing transgenic Arabidopsis thaliana lines A: Growth conditions of various lines after treatment with 0 and 100 mmol/L NaCl for 7 d. B: Statistical analysis of root length of various lines after treatment with 0 and 100 mmol/L NaCl for 7 d

图8 SmERF B3-45在拟南芥中过表达增强植物对盐胁迫的抗性

Fig. 8 Overexpression of SmERF B3-45 in transgenic Arabidopsis enhancing its tolerance to salt

图9 SmERF B3-45沉默降低柳树对盐胁迫的抗性 A：转基因植株中SmERF B3-45的表达；B：100 mmol/L NaCl处理后，植株的生长情况，红色箭头所示叶片出现严重萎蔫、枯萎和凋落现象；C：总蛋白含量；D：MDA含量；E：脯氨酸含量。pTRV2：阴性对照植株；pTRV2- SmERF B3-45-1、pTRV2- SmERF B3-45-2、pTRV2- SmERF B3-45-3为基因沉默植株

Fig. 9 Silencing SmERF B3-45 through VIGS compromised the tolerance in willow to salt A: Expression of SmERF B3-45 in transgenic plants. B: Growth condition of plants after treatment with 100 mmol/L NaCl, where the red arrows indicate severe wilting, withering, and leaf drop phenomena. C: Total protein content. D: MDA content. E: Proline content. pTRV2: Negative control plants. pTRV2-SmERF B3-45-1, pTRV2-SmERF B3-45-2, pTRV2-SmERF B3-45-3: Gene-silenced plants

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