玉米大斑病菌热激蛋白HSP 9/12基因的克隆与表达分析

doi:10.3864/j.issn.0578-1752.2025.18.006

中国农业科学 ›› 2025, Vol. 58 ›› Issue (18): 3648-3663.doi: 10.3864/j.issn.0578-1752.2025.18.006

玉米大斑病菌热激蛋白HSP 9/12基因的克隆与表达分析

张淑红¹(), 高凤菊¹, 武秋颖¹, 纪景欣¹, 张运峰¹, 许可¹, 谷守芹², 范永山¹()

¹ 唐山师范学院生命科学系/河北省植物生物技术研究与应用重点实验室/唐山市农业病原真菌与毒素重点实验室，河北唐山 063000
² 河北农业大学生命科学学院/河北省农业微生物生物信息利用技术创新中心，河北保定 071000

收稿日期:2025-05-18 接受日期:2025-06-15 出版日期:2025-09-18 发布日期:2025-09-18
通信作者:
范永山，E-mail：fanyongshan@126.com
联系方式: 张淑红，E-mail：zsh3535@163.com。
基金资助:
国家自然科学基金(22078171); 中央引导地方科技发展资金(246Z3610G); 唐山市科技计划(23130221E); 唐山师范学院科研项目(20256129033)

Cloning and Expression Analysis of Heat Shock Protein HSP 9/12 Genes in Setosphaeria turcica

ZHANG ShuHong¹(), GAO FengJu¹, WU QiuYing¹, JI JingXin¹, ZHANG YunFeng¹, XU Ke¹, GU ShouQin², FAN YongShan¹()

¹ Department of Life Sciences, Tangshan Normal University/Hebei Key Laboratory of Plant Biotechnology Research and Application/ Tangshan Key Laboratory of Agricultural Pathogenic Fungi and Toxins, Tangshan 063000, Hebei
² College of Life Sciences, Hebei Agricultural University/Hebei Bioinformatic Utilization and Technological Innovation Center for Agricultural Microbes, Baoding 071000, Hebei

Received:2025-05-18 Accepted:2025-06-15 Published:2025-09-18 Online:2025-09-18

摘要/Abstract

摘要：

【目的】克隆玉米大斑病菌（Setosphaeria turcica）非ACD结构域类小分子热激蛋白HSP 9/12基因，分析其在病菌发育、侵染和HT-毒素诱导过程中的表达模式。【方法】在玉米大斑病菌全基因组范围内筛选并克隆热激蛋白HSP 9/12基因，利用生物信息学方法进行编码蛋白的理化性质分析、亚细胞定位、结构预测和系统发育分析，利用RNA-seq和RT-qPCR分析HSP 9/12基因在玉米大斑病菌发育、侵染和HT-毒素诱导过程中的表达情况。【结果】从玉米大斑病菌基因组筛选并克隆到两个HSP 9/12基因，其编码蛋白分别含有99和100个氨基酸，根据分子量分别命名为StHsp10.1和StHsp10.7。理化性质分析表明，两个HSP 9/12均为亲水蛋白，亚细胞定位预测均为细胞质并含有核定位信号，无跨膜结构域和信号肽，均含有HSP9_HSP12（PF04119）结构域；StHSP10.1为酸性不稳定蛋白，StHSP10.7为碱性稳定蛋白，均以α-螺旋为主导的二级和三级结构形式存在；StHSP10.1与酿酒酵母（Saccharomyces cerevisiae）HSP12亲缘关系较近，StHSP10.7与粟酒裂殖酵母（Schizosaccharomyces pombe）HSP9亲缘关系较近。StHSP10.1在分生孢子发育期表达量最高，其次为菌丝、附着胞和侵入钉，芽管表达量较低；玉米大斑病菌接种后StHSP10.1表达量迅速上升，接种72 h时的FPKM达到接种24 h的6.37倍；HT-毒素诱导过程中的RT-qPCR分析结果表明，随着诱导时间增加，StHSP10.1在野生型菌株（WT）中相对基因表达量显著上升，诱导14、21和28 d分别为7 d的2.9、14.1和39.8倍，但在STK1基因敲除突变体（ΔSTK1）中表达量均极低；StHSP10.7在玉米大斑病菌发育阶段、侵染过程和HT-毒素诱导过程中均表达量极低。AlphaFold 3预测显示，StHSP10.1转录起始位点上游-38—-24 bp区域同时存在TATA-box、细胞分化蛋白RCD1结合位点和bZIP转录因子StbZIP11结合位点；利用STRING在线网站构建StHSP10.1蛋白质互作网络，发现2条StHSP10.1调控路径：Ras1→STK1→StbZIP11→StHSP10.1和Ras1→UBE2→CUE1→RCD1-like→StHSP10.1，推测分别在HT-毒素合成和胁迫诱导方面发挥重要作用。【结论】玉米大斑病菌HSP 9/12基因的表达模式存在显著差异，StHSP10.1是病菌发育、侵染和HT-毒素诱导过程中的关键调控基因，而StHSP10.7无调控作用。

关键词: 玉米大斑病菌, HSP 9/12, 小分子热激蛋白, 基因克隆, 转录调控

Abstract:

【Objective】The objective of this study is to clone HSP 9/12 genes of small heat shock proteins without ACD domain from Setosphaeria turcica and analyze their expression patterns during fungal development, infection, and HT-toxin induction processes. 【Method】The coding genes of heat shock protein HSP 9/12 were screened and cloned from the whole genome of S. turcica. Bioinformatics methods were employed to analyze the physicochemical properties, subcellular localization, structural prediction, and phylogenetic analysis of HSP 9/12 proteins. RNA-seq and RT-qPCR were used to examine the expression of HSP 9/12 genes during fungal development, infection, and HT-toxin induction. 【Result】Two HSP 9/12 genes were screened and cloned from the S. turcica genome, encoding proteins with 99 and 100 amino acids, respectively. Based on their molecular weights, they were named StHsp10.1 and StHsp10.7. Physicochemical analysis revealed that both HSP 9/12 proteins are hydrophilic, with subcellular localization predictions indicating they are located in the cytoplasm with nuclear localization signals. They lack transmembrane domains and signal peptides, and both contain the HSP9_HSP12 (PF04119) domain. StHSP10.1 is an acidic unstable protein, while StHSP10.7 is an alkaline stable protein, both existing predominantly in α-helix-dominated secondary and tertiary structural forms. StHSP10.1 shows closer phylogenetic relationship with Saccharomyces cerevisiae HSP12, whereas StHSP10.7 exhibits closer affinity to Schizosaccharomyces pombe HSP9. The StHSP10.1 exhibited the highest expression during conidial development, followed by hypha, appressoria, and penetration peg, with the lowest expression in germ tubes. After inoculation, the fungal StHSP10.1 expression rapidly increased, reaching 6.37-fold higher FPKM at 72 h compared to 24 h post inoculation. The results of RT-qPCR analysis during the HT-toxin induction process showed that, as the induction time increased, the relative gene expression level of StHSP10.1 in the wild-type strain (WT) significantly increased being 2.9-, 14.1-, and 39.8-fold higher at 14, 21, and 28 d compared to 7 d, respectively, but remained extremely low in the STK1 gene knockout mutant (ΔSTK1). StHSP10.7 showed extremely low expression levels during fungal development, infection, and HT-toxin induction. AlphaFold 3 predicted that the region from -38 to -24 bp upstream of the transcription start site of the StHSP10.1 contains TATA-box, and binding sites for cell differentiation proteins RCD1 and bZIP transcription factor StbZIP11, simultaneously. Using the STRING online platform to construct the protein-protein interaction network for StHSP10.1, two regulatory pathways of StHSP10.1 were proposed: Ras1→STK1→StbZIP11→StHSP10.1 and Ras1→UBE2→CUE1→RCD1-like→StHSP10.1, suggesting important roles in HT-toxin synthesis and stress induction, respectively. 【Conclusion】There are significant differences in the expression patterns of HSP 9/12 genes in S. turcica. StHSP10.1 serves as a key regulatory gene in the processes of pathogen development, infection, and HT-toxin induction, whereas StHSP10.7 has no regulatory effect.

Key words: Setosphaeria turcica, HSP 9/12, small heat shock protein (sHSP), gene cloning, transcriptional regulation

张淑红, 高凤菊, 武秋颖, 纪景欣, 张运峰, 许可, 谷守芹, 范永山. 玉米大斑病菌热激蛋白HSP 9/12基因的克隆与表达分析[J]. 中国农业科学, 2025, 58(18): 3648-3663.

ZHANG ShuHong, GAO FengJu, WU QiuYing, JI JingXin, ZHANG YunFeng, XU Ke, GU ShouQin, FAN YongShan. Cloning and Expression Analysis of Heat Shock Protein HSP 9/12 Genes in Setosphaeria turcica[J]. Scientia Agricultura Sinica, 2025, 58(18): 3648-3663.

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引物名称 Primer name	基因特异性引物序列 Gene specific primer sequence (5′-3′)	引物名称 Primer name	表达分析用引物序列 Sequence for gene expression analysis (5′-3′)
StHSP10.1 F	ATGTCTGACTCCATGCGCAA	StHSP10.1 qF	CAGGCCTCGGAGAAGATCAC
StHSP10.1 R	TTACTTCTTCTGGCCGCCAG	StHSP10.1 qR	CACGCCGGAGCTCTTGTTAG
StHSP10.7 F	ATGACCTCTGCCTTCCGC	StHSP10.7 qF	CTCGGTGAAGCAATGCAACC
StHSP10.7 R	TTACAACCCATTCCCATGCG	StHSP10.7 qR	CACATTGCGGTCGTAGGAGC
		β-tubulin qF	CAACGAAGCCTCCAACAACA
		β-tubulin qR	CTCGGTGTAGTGACCCTTTGC

项目Item	StHSP10.1	StHSP10.7
氨基酸数目Number of amino acids	99	100
等电点pI	4.98	9.65
疏水性系数Grand average of hydropathicity	-1.06	-1.04
不稳定系数Instability index	44.95	23.63
亚细胞定位Subcellular localization	细胞质Cytoplasm（可能性Probability 0.7207>阈值Threshold 0.4761）	细胞质Cytoplasm（可能性Probability 0.7646>阈值Threshold 0.4761）
	细胞核Nucleus（可能性Probability 0.4289<阈值Threshold 0.5014）	细胞核Nucleus（可能性Probability 0.4142<阈值Threshold 0.5014）
	膜关联Membrane association：可溶Soluble（可能性Probability 0.604>阈值Threshold 0.500）	膜关联Membrane association：外周Peripheral（可能性Probability 0.730>阈值Threshold 0.600），可溶Soluble（可能性Probability 0.660>阈值Threshold 0.500）
	核定位信号Nuclear localization signal	核定位信号Nuclear localization signal

HSP 9/12	α-螺旋α-helix		无规则卷曲Random coil
HSP 9/12	数目Number	比例Ratio (%)	数目Number	比例Ratio (%)
StHSP10.1	71	71.72	28	28.28
StHSP10.7	61	61.00	39	39.00

蛋白质ID Protein ID	相关系数 r_pearson	相关系数P值 <BOLD>P </BOLD>val_pearson	注释 Annotation
178071	0.9620	6.79E-14	PF00583乙酰转移酶（GNAT）家族Acetyltransferase (GNAT) family
162963	0.9513	9.83E-13	PF04082真菌特异性转录因子结构域Fungal specific transcription factor domain
168401	0.9352	2.13E-11	PF00397 WW结构域WW domain
111166	0.9237	1.22E-10	PF07716碱性亮氨酸拉链Basic region leucine zipper
184968	0.9208	1.81E-10	KOG2422未表征的保守蛋白Uncharacterized conserved protein
39934	0.9204	1.92E-10	KOG2177预测的E3泛素连接酶Predicted E3 ubiquitin ligase
181354	0.9150	3.83E-10	KOG3036参与细胞分化/有性发育的蛋白质Protein involved in cell differentiation/ sexual development PF04078细胞分化家族，RCD1样蛋白Cell differentiation family, RCD1-like
1022253	0.9027	1.60E-09	PF00856 SET结构域SET domain
162257	0.9009	1.95E-09	PF13523乙酰转移酶（GNAT）结构域Acetyltransferase (GNAT) domain

作用顺式元件cis-regulatory element	数目Number
Short_function	31
参与茉莉酸甲酯响应的顺式作用调控元件cis-acting regulatory element involved in the MeJA-responsiveness	20
参与光响应性的顺式作用调控元件cis-acting regulatory element involved in light responsiveness	9
启动子和增强子区域常见的顺式作用元件Common cis-acting element in promoter and enhancer regions	8
参与脱落酸响应的顺式作用元件cis-acting element involved in the abscisic acid responsiveness	7
转录起始位点上游约-30处的核心启动子元件Core promoter element around -30 of transcription start site	7
光响应元件的一部分Part of a light responsive element	4
光响应元件Light responsive element	3
生长素响应元件Auxin-responsive element	1
参与低温响应的顺式作用元件cis-acting element involved in low-temperature responsiveness	1
参与干旱诱导性的MYB结合位点MYB binding site involved in drought-inducibility	1
MYBHv1结合位点MYBHv1 binding site	1

玉米大斑病菌热激蛋白HSP 9/12基因的克隆与表达分析

Cloning and Expression Analysis of Heat Shock Protein HSP 9/12 Genes in Setosphaeria turcica

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基因名称 Gene name	蛋白质ID Protein ID	相关系数 r_pearson	相关系数P值 <BOLD>P</BOLD>val_pearson	注释 Annotation	Cluster
STK1	47519	0.4551	0.0254	cd07856 STKc_Sty1_Hog1	1
Ras1	169673	0.5297	0.0077	PF00071 Ras1	1
StbZIP11	155297	0.4830	0.0167	IPR004827 bZIP	1
UBE2	92314	0.3633	0.0809	PF00179泛素结合酶Ubiquitin-conjugating enzyme	2
CUE1	172535	0.7563	1.90E-05	IPR040192 CUE结构域蛋白1 CUE domain-containing protein 1	2
RCD1-like	181354	0.9150	3.83E-10	PF04078细胞分化家族，Rcd1样蛋白Cell differentiation family, Rcd1-like	2
Ish1	77830	0.6733	0.0003	IPR018803 Ish1/Msc1-like	3
Sdo1	162233	0.9381	1.30E-11	PF09377 SBDS蛋白质结构域II SBDS protein domain II	3
Gad1	125179	0.7178	7.85E-05	IPR010107谷氨酸脱羧酶Glutamate decarboxylase	3
StHSP10.7	26210	0.4599	0.0237	PF04119热激蛋白9/12 Heat shock protein 9/12 HSP 9_HSP12	3
GH63	166579	0.0178	0.9342	IPR004888糖苷水解酶家族63 Glycoside hydrolase family 63	3
AGP1	169279	-0.6122	0.0014	IPR011834 α-葡聚糖磷酸化酶Alpha-glucan phosphorylase	4
PGM1	95885	0.2355	0.2678	PTHR45955磷酸己糖异构酶Phosphohexose mutase	4
Gtf20	174551	-0.4498	0.0273	PF00982糖基转移酶家族20 Glycosyltransferase family 20	4
CBM32	165151	0.2612	0.2175	PF18344碳水化合物结合模块家族32 Carbohydrate binding module family 32	4
TPS1	164742	-0.4354	0.0334	cd03788海藻糖-6-磷酸合成酶Trehalose-6-phosphate synthase	4

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