杜仲EuGIF1基因鉴定及其表达和蛋白互作分析

doi:10.13560/j.cnki.biotech.bull.1985.2025-0438

生物技术通报 ›› 2025, Vol. 41 ›› Issue (12): 267-279.doi: 10.13560/j.cnki.biotech.bull.1985.2025-0438

杜仲EuGIF1基因鉴定及其表达和蛋白互作分析

王若若¹^,²(), 曲鹏坤¹, 张欣¹, 王珞¹, 朱英¹, 田双一³, 赵德刚²^,⁴()

^1.贵州省生物技术研究所，贵阳 550006
^2.贵州省农业科学院植物保育技术应用工程研究中心，贵阳 550006
^3.贵州师范学院生物科学学院，贵阳 550018
^4.贵州大学生命科学学院农业生物工程研究院山地植物资源保护与种质创新教育部重点实验室，贵阳 550025

收稿日期:2025-04-24 出版日期:2025-12-26 发布日期:2026-01-06
通讯作者: 赵德刚，男，博士，教授，研究方向：杜仲功能基因及高值利用；E-mail: dgzhao@gzu.edu.cn
作者简介:王若若，女，博士，助理研究员，研究方向：植物功能基因；E-mail: ruozhu_w@163.com
基金资助:
贵州省基础研究（自然科学）计划项目（黔科合基础-ZK［2024］一般532），贵州省科技支撑计划项目（黔科合支撑［2025］一般 083），贵州省农业科学院青年科技基金项目(黔农科博士基金［2024］06);贵州省农业科学院人才专项项目(黔农科人才专项［2024］02);贵州省农业科学院青年科技基金项目(黔农科一般基金［2025］24)

Molecular Characterization， Expression Profiling， and Protein Interaction Analysis of the EuGIF1 Gene in Eucommia ulmoides

WANG Ruo-Ruo¹^,²(), QU Peng-Kun¹, ZHANG Xin¹, WANG Luo¹, ZHU Ying¹, TIAN Shuang-Yi³, ZHAO De-Gang²^,⁴()

^1.Guizhou Institute of Biotechnology, Guiyang 550006
^2.Plant Conservation Technology Center, Guizhou Academy of Agricultural Sciences, Guiyang 550006
^3.College of Biological Sciences, Guizhou Normal University, Guiyang 550018
^4.The Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region, Ministry of Education, Institute of Agricultural Bioengineering, College of Life Sciences, Guizhou University, Guiyang 550025

Received:2025-04-24 Published:2025-12-26 Online:2026-01-06

摘要/Abstract

摘要：

目的基于杜仲（Eucommia ulmoides Oliv.）全基因组数据，系统鉴定GIF（GRF-interacting factor）基因家族成员，分析GIF基因家族成员基因表达模式及蛋白互作特性，为解析杜仲器官发育调控网络及优化杜仲的遗传转化体系提供理论依据。方法利用HMMER和BLASTP方法鉴定杜仲GIF基因家族成员，结合生物信息学工具分析蛋白理化性质、三维结构及启动子顺式元件；通过RT-qPCR检测基因组织特异性及赤霉素GA₃诱导表达模式；采用酵母双杂交（Y2H）和双分子荧光互补（BiFC）实验验证EuGIF1与EuGRF5的互作关系；此外，用EuGIF1基因的过表达载体对拟南芥gif1突变体进行遗传互补。结果在杜仲的基因组中共鉴定到了3个EuGIF基因，EuGIF1、EuGIF2和EuGIF3，其中，EuGIF1和EuGIF2位于杜仲基因组的7号染色体，EuGIF3位于杜仲基因组的17号染色体。EuGIF1、EuGIF2和EuGIF3编码的蛋白均含保守的SSXT/SNH结构域。启动子序列分析显示，EuGIF1基因的启动子区域含有2个赤霉素响应元件。EuGIF1在顶端分生组织中高表达且受赤霉素GA₃快速诱导；蛋白的三维结构预测显示SSXT/SNH结构域可形成蛋白互作界面。共表达分析表明EuGIF1与EuGRF1/3/5表达模式相似，但Y2H和BiFC实验均未检测到EuGIF1与EuGRF5的直接互作。此外，EuGIF1基因在拟南芥中的过表达无法互补拟南芥gif1突变体中叶片窄小的表型。结论 EuGIF1可能在赤霉素信号介导的杜仲器官发育中发挥重要作用，GIF1与GRF的互作可能具有物种特异性，且基因功能的保守性在不同物种之间存在一定的局限性。

关键词: 杜仲, GIF基因家族, 赤霉素, 蛋白三维结构, GRF蛋白, 蛋白质相互作用

Abstract:

Objective To systematically identify the GIF gene family in Eucommia ulmoides and analyze their expression patterns and protein interaction characteristics, aiming to decipher the regulatory network of organ development and optimize genetic transformation strategies. Method HMMER and BLASTPwere used to identify GIF genes in Eucommia ulmoides. Bioinformatics tools were employed to analyze protein physicochemical properties, 3D structures, and promoter cis-elements. RT-qPCR was adapted to validate the tissue-specific and GA₃-induced expression of EuGIF1. Yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays were conducted to verify the interaction between EuGIF1 and EuGRF5. Additionally, the overexpression vector carrying the EuGIF1 gene was to genetically complement the gif1 mutant of Arabidopsis thaliana. Result Three EuGIF genes EuGIF1/2/3 with conserved SSXT/SNH domains were identified in E. ulmoides. EuGIF1 and EuGIF2 were located on chromosome 7 of the E. ulmoides genome, and EuGIF3 was located on chromosome 17. The proteins encoded by EuGIF1,EuGIF2 and EuGIF3 all contained conserved SSXT/SNH domain.Promoter sequence analysis revealed that the promoter region of the EuGIF1 gene contained two gibberellin-response elements. EuGIF1 had high expression in apical meristems and rapid induction by GA₃. 3D structural prediction of the protein revealed potential interaction interfaces between the SSXT/SNH domains. Co-expression analysis suggested functional synergy between EuGIF1 and EuGRF1/3/5, but Y2H and BiFC assays showed no direct interaction between EuGIF1 and EuGRF5. The overexpression of EuGIF1 in A. thalianagif1 mutant failed to complement its narrow-leaf phenotype. Conclusion EuGIF1 may play a significant role in gibberellin-mediated organ development in E. ulmoides, whereas its interaction with GRFs shows species specificity. Furthermore, the functional conservation of this gene appears limited across divergent species.

Key words: Eucommia ulmoides, GIF gene family, gibberellin, protein 3D-structure, GRF protein, protein-protein interaction

王若若, 曲鹏坤, 张欣, 王珞, 朱英, 田双一, 赵德刚. 杜仲EuGIF1基因鉴定及其表达和蛋白互作分析[J]. 生物技术通报, 2025, 41(12): 267-279.

WANG Ruo-Ruo, QU Peng-Kun, ZHANG Xin, WANG Luo, ZHU Ying, TIAN Shuang-Yi, ZHAO De-Gang. Molecular Characterization， Expression Profiling， and Protein Interaction Analysis of the EuGIF1 Gene in Eucommia ulmoides[J]. Biotechnology Bulletin, 2025, 41(12): 267-279.

图/表 11

表1 引物序列表

Table 1 Table of primer sequences

引物名称 Primer name	序列 Sequence （5′‒3′）
cdsEuGIF1-F	ctagaggatctcgaggcATGCAGCAGCACCTGATG
cdsEuGIF1-R	cgtctgtacacctaggTCAGTTTCCATCATCAGAA
EuGIF1gfp-F	ttggagaggacacgcATGCAGCAGCACCTGATG
EuGIF1gfp-R	cttctcccttacccatGTTTCCATCATCAGAAGCCT
YN-GIF1-F	gcatttaaatctcgaggATGCAGCAGCACCTGATG
YN-GIF1-R	gtggcgatggatcttctGTTTCCATCATCAGAAGC
YC-GRF5-F	gaggaggacctgctttATGAACGTGAACGCGATGA
YC-GRF5-R	acgccggacgggtaccgCCAGTAGGGTCTGGAGT
AD-GIF1-F	ggccatggaggccagtATGCAGCAGCACCTGATG
AD-GIF1-R	gcagctcgagctcgatGTTTCCATCATCAGAAGCC
BD-GRF5-F	tatggccatggaggccATGAACGTGAACGCGATGA
BD-GRF5-R	gccgctgcaggtcgacCCAGTAGGGTCTGGAGTT
YS22-GFP-R	aggaagctttccagtagtgca
termi-R	aagaccggcaacaggattc
cdsEuGIF1-F2	CAGCTGGGAATGAGCTCTGG
EuGIF1-qRT-F	CAGCAGTATTCGGCACTACAG
EuGIF1-qRT--R	CCTCCACTCCCACCCATT
EuGIF2-qRT--F	CCATCACCAGCAGCATCAAT
EuGIF2-qRT--R	CACCGCCACCTCCGATAT
EuGIF3-qRT--F	ACAATGGCTCAGCAACAACA
EuGIF3-qRT--R	GTGGTGGAAGTGGAGTAGGT
EuACTIN-qRT--F	GTGTTATGGTTGGGATGGG
EuACTIN-qRT--R	TGCTGACTATGCCGTGTTC

图1 杜仲EuGIFs蛋白序列分析及基因在染色体上的分布A：EuGIFs蛋白序列中保守结构域的分布；B：EuGIFs蛋白的氨基酸序列比对；C：EuGIFs基因在染色体上的分布

Fig. 1 Distribution of conserved domains in the EuGIFs protein sequences and chromosomal distribution of the genes in E. ulmoidesA: Distribution of conserved domains in the EuGIFs protein sequences. B: Amino acid sequence alignment of EuGIFs proteins. C: Chromosomal distribution of the EuGIFs genes

表2 杜仲EuGIFs蛋白理化性质

Table 2 Physicochemical properties of the EuGIFs proteins in E. ulmoides

基因

名称

Gene name

基因ID

Gene ID

氨基酸长度

Number of amino acids （aa）

蛋白分子量

Molecular weight （Da）

等电点

Theoretical pI

不稳定指数

Instability index

脂肪族氨基酸指数

Aliphatic index

疏水性平均值

Grand average of hydropathicity

亚细胞定位

Subcellular location

EuGIF1

EuGIF2

EuGIF3

图2 EuGIFs蛋白的三维空间结构图A：EuGIFs蛋白的三维结构的卡通图；箭头指向的区域为SSXT/SNH结构域的区域；B：EuGIFs蛋白的三维表面结构图；箭头指示的是pLDDT值大于90的氨基酸，对应A图中棍状结构显示的氨基酸

Fig. 2 Three-dimensional spatial structure diagram of the EuGIFs proteinA: Cartoon representation of the 3D structure of EuGIFs protein. Regions corresponding to the SSXT/SNH domains are indicated by arrows. B: Surface representation of the 3D structure of EuGIFs protein. The arrows denote the amino acids with pLDDT (predicted local distance difference test) values>90, which correspond to the amino acids depicted as stick structures in Fig. A

图3 杜仲EuGIFs基因启动子上响应元件的数量（A）和分布情况（B）

Fig. 3 Number (A) and distribution (B) of response elements on the promoter of the EuGIFs gene in E. ulmoides

图4 杜仲EuGIFs基因的表达模式A：杜仲EuGIFs基因在杜仲各组织部位的表达情况；B：杜仲幼苗在喷施GA3后，幼叶中EuGIFs基因的表达情况；***P<0.001、ns表示没有显著差异（P>0.05）

Fig. 4 Expression pattern of EuGIFs genes in E. ulmoidesA: Expression profiles of the EuGIFs gene in different tissues of E. ulmoides. B: Expression profiles of the EuGIFs gene in young leaves of seedlings following exogenous GA3 treatment. *** P<0.001, ns indicates no statistically significant difference (P>0.05)

图5 GIF同源蛋白的系统发育分析及EuGIF与EuGRFs的基因共表达模式A：基于蛋白序列全长构建的邻接法系统进化树；所有蛋白均包含保守的SNH/SSXT结构域，绿色阴影部分为AtGIF1的同源蛋白，红色标注的是EuGIF1；蛋白名称中的物种缩写Eu、Cc、At、Vv、Cl、Fve、Os、Ta分别对应杜仲、柑橘、拟南芥、葡萄、西瓜、二倍体野生草莓、水稻、普通小麦；B：EuGIFs和EuGRFs的基因表达模式；红虚线框表示分生组织高表达且模式相似的基因，颜色梯度表示表达量（蓝‒黄‒红：低‒中‒高）

Fig. 5 Phylogenetic analysis of GIF homologs and gene co-expression profiles of EuGIF and EuCRFsA: Neighbor-joining phylogenetic tree constructed using full-length protein sequences, with all proteins containing the conserved SNH/SSXT domain. The green-shaded region highlights AtGIF1 homologs, and EuGIF1 is marked in red. The species abbreviations in the protein names, Eu, Cc, At, Vv, Cl, Fve, Os, and Ta, correspond to Eucommia ulmoides, Citrus clementina, Arabidopsis thaliana, Vitis vinifera, Citrullus lanatus, Fragaria vesca, Oryza sativa, and Triticum aestivum, respectively. B: Expression patterns of EuGIFs and EuGRFs, with the red dashed box indicating genes having high and correlated expression in meristematic tissues. The color gradient (blue-yellow-red) indicate expression levels (low-medium-high) of EuGRFs

图6 GFP融合蛋白在烟草叶片下表皮细胞中的亚细胞定位图中展示4个成像通道：GFP（绿色，激发光/发射光：488/510 nm）、叶绿体自发荧光（红色，激发光/发射光：640/675 nm）、明场和合并图像。图中比例尺均为50 μm

Fig. 6 Subcellular localization of GFP-tagged proteins in the epidermal cells of tobacco leafThe figure displays four imaging modalities: GFP fluorescence (green, excitation/emission: 488/510 nm); chloroplast autofluorescence (red, excitation/emission: 640/675 nm); bright field (grayscale) and merged image. Scale bar: 50 μm

表3 用HDOCK预测的EuGIF1-EuGRF5蛋白互作结构分析结果

Table 3 Structural analysis of EuGIF1-EuGRF5 protein-protein interaction predicted by HDOCK

蛋白模型编号 Number	结构偏差 RMSD （Å）	亲和力 Score
1	50.52	-809.33
2	31.22	-774.96
3	69.01	-764.03
4	60.97	-758.89
5	55.71	-755.58
6	79.41	-749.46
7	64.33	-747.77
8	62.85	-735.99
9	62.97	-732.66
10	68.86	-732.20

图7 EuGIF1与EuGRF5的酵母双杂交互作验证SD/-LT：亮氨酸（-L）和色氨酸（-T）双重缺陷型合成培养基；SD/-LTAH/X-α-Gal：添加5-溴-4-氯-3-吲哚基-α-D-吡喃半乳糖苷的四重缺陷型（-L/-T/-A/-H）严格筛选培养基；图上标注的OD600值（0.2、0.02、0.002、0.000 2）代表点种实验前酵母的10倍梯度稀释浓度；阳性对照组：BD-P53+AD-T；阴性对照组1：BD-Lam+AD-T，结果与阳性对照组结合验证实验室实验系统的稳定性；实验组：BD-EuGRF5+AD-EuGIF1；阴性对照组2：BD-EuGRF5+AD/BD+AD-EuGIF1

Fig. 7 Yeast two-hybrid assay for protein-protein interaction between EuGIF1 and EuGRF5SD/-LT: Synthetic dropout medium deficient in leucine (-L) and tryptophan (-T). SD/-LTAH/X-α-Gal: Stringent selection medium with quadruple dropout (-L/-T/-A/-H) supplemented with 5-bromo-4-chloro-3-indolyl-α-D-galactopyranoside (X-α-Gal). The indicated OD600 values (0.2, 0.02, 0.002, and 0.000 2) represent 10-fold serial dilutions of yeast cultures prior to spotting assay. Positive control: BD-P53+AD-T; negative control 1: BD-Lam+AD-T; test group: BD-EuGRF5+AD-EuGIF1; negative control 2: BD-EuGRF5+AD/BD+AD-EuGIF1

图8 EuGIF1对拟南芥gif1突变体的遗传互补A：遗传互补的T3代转基因植株的基因型鉴定结果；B：培养基上T3代转基因植株12 d的幼苗表型，箭头指示野生型、突变体及3株具有代表性的T3代纯合阳性转基因株系的幼叶，图中比例尺均为0.5 cm

Fig. 8 Genetic complementation of the A. thalianagif1 mutant by EuGIF1A: Genotyping results of T3 generation transgenic plants for the complementation test. B: Phenotypic characterization of 12 d T3 transgenic seedlings grown in medium, with arrows indicating the wild type, mutant, and three representative T3 homozygous positive transgenic lines for juvenile leaves. Scale bar: 0.5 cm

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杜仲EuGIF1基因鉴定及其表达和蛋白互作分析

Molecular Characterization， Expression Profiling， and Protein Interaction Analysis of the EuGIF1 Gene in Eucommia ulmoides

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