Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (18): 3648-3663.doi: 10.3864/j.issn.0578-1752.2025.18.006

• PLANT PROTECTION • Previous Articles     Next Articles

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. 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 Online:2025-09-18 Published:2025-09-18
  • Contact: FAN YongShan

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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

Table 1

The sequence of primers"

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

Fig. 1

PCR amplification (A) and structure analysis (B) of HSP 9/12 genes in S. turcica M: DL1000 DNA Marker; 1: StHSP10.1 DNA; 2: StHSP10.1 cDNA; 3: StHSP10.7 cDNA; 4: StHSP10.7 DNA"

Fig. 2

Homology alignment (A), structure analysis (B) and conserved motif Logo (C) of HSP 9/12 in S. turcica"

Table 2

Physicochemical properties and subcellular localization prediction of HSP 9/12 in S. turcica"

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

Table 3

Secondary structure prediction of HSP 9/12 in S. turcica"

HSP 9/12 α-螺旋α-helix 无规则卷曲Random coil
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

Fig. 3

Prediction of tertiary structure model of HSP 9/12 in S. turcica and two yeast species"

Fig. 4

Phylogenetic analysis of fungal HSP 9/12"

Fig. 5

Expression of HSP 9/12 genes during development stages (A) and infection process (B) in S. turcica *: P<0.05; **: P<0.01"

Fig. 6

Expression of HSP 9/12 genes during HT-toxin induction in S. turcica"

Table 4

Transcription factors with the positive correlation coefficient greater than 0.9 for StHSP10.1 expression"

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

Fig. 7

Interaction prediction of StHSP10.1 promoter sequences with transcription factors RCD1-like and StbZIP11"

Table 5

Upstream cis-regulatory elements prediction of the StHSP10.1"

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

Fig. 8

Protein-protein interaction network of the StHSP10.1"

Fig. 9

Interacting protein prediction of StHSP10.1, STK1, CUE1 and Ras1 in S. turcica using AlphaFold 3"

Table 6

Information of genes in protein-protein interaction networks of StHSP10.1"

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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