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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (12): 1850-1861.doi: 10.3724/SP.J.1006.2020.04004


Molecular cloning and expression analysis of BoGSTL21 in self-incompatibility Brasscia oleracea

Tong-Hong ZUO1(), He-Cui ZHANG1, Qian-Ying LIU1, Xiao-Ping LIAN2, Qin-Qin XIE1, Deng-Ke HU1, Yi-Zhong ZHANG1, Yu-Kui WANG1, Xiao-Jing BAI1, Li-Quan ZHU1,*()   

  1. 1College of Agronomy and Biotechnology, Southwest University, Chongqing 400716, China
    2College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400716, China
  • Received:2020-01-08 Accepted:2020-07-02 Online:2020-12-12 Published:2020-09-24
  • Contact: Li-Quan ZHU E-mail:zuotongh@163.com;zhuliquan@swu.edu.cn
  • Supported by:
    National Natural Science Foundation of China(31572127);Chongqing Graduate Research and Innovation Project(CYS18085);Basic Scientific Research Business Expenses Project of the Central University(XDJK2017C032)


Glutathione-S-transferase (GSTs) plays an important role in plant resistance to stress, cytotoxic release and plant growth and development. In this study, we identified an up-regulated gene named BoGSTL21 based on the stigma transcriptome data in 0-60 min self-pollination. BoGSTL21 had an open reading frame (ORF) with the length of 900 bp, encoded a protein of 299 amino acid residues, which contained GST-N and GST-C domains without signal peptide and transmembrane domain, the theory isoelectric point of BoGSTL21 was 8.49. The promoter of BoGSTL21 gene contained many cis-acting elements such as light response, auxin response, abscisic acid response, low temperature and drought response. BoGSTL21 expresses in different tissues of Brassica oleracea. The expression level in stigma varies with developmental time, and was mainly overexpressed in mature stigma. The results of qRT-PCR revealed that BoGSTL21 mRNA expression level after self-and cross-pollinations for 0 min to 60 min was consistent with that of RNA-seq data. It was found through yeast two-hybrid that BoGSTL21 protein interacted with pollen development-related protein BoFAB1C, auxin-related protein BoPATL2, and aldolase-type TIM barrel family protein BoF9N12_9. BoGSTL21 gene was successfully induced and expressed in E. coli BL21 (DE3) with a purified protein size of 34 kD, which was consistent with the predicted results. According to the above results, BoGSTL21 may be a novel protein involved in the SI response process, which provides a new content for further research and utilization of self-incompatibility in Brasscia oleracea.

Key words: Brassica oleracea, gene cloning, self-incompatibility, expression analysis, yeast two-hybrid

Table 1

Primers used in gene cloning and qRT-PCR"

Primer name
Primer sequence (5°-3°)
R: CAAGCACAATACCAGTAGTAC Internal reference primers
Yeast two-hybrid primers

Fig. 1

Analysis of expression patterns of BoGSTL21 after self-pollination and cross-pollination using stigma transcriptome data SP: self-pollination; CP: cross-pollination."

Fig. 2

Amplification product electrophoresis of BoGSTL21 cDNA and gDNA sequences in Brassica oleracea"

Fig. 3

Gene structure of Brassica oleracea BoGSTL21 and its deduced amino acid sequence The dotted box denotes the N-glycosylation site, the solid line frame denotes the GST-N domain, and the underlined line denotes the GST-C domain."

Fig. 4

Phylogenetic tree of BoGSTL21 and other species GSTL2 amino acid sequences"

Fig. 5

Alignment of BoGSTL21 of Brassica oleracea with homologous proteins of other species Black: amino acid identity 100%; Dark gray: amino acid identity 75%; White: amino acid identity 50%. The triangle marks the difference between BoGSTL21 and BoGSTL2; the underlined line denotes the GST-N terminal domain, and the underlined line denotes the GST-C terminal domain, which also indicates that the protein is highly conserved in this segment."

Table 2

Cis-elements in the upstream regulation region of BoGSTL21"

Associated putative function
Cis-elements in the promoter region
脱落酸(ABA)应答 Abscisic acid response ABRE
光响应 Light response G-Box, GT1-motif, TCT-motif
低氧诱导 Anaerobic induction response ARE
促进和增强基因转录 Promote and enhance gene transcription CAAT-box
赤霉素应答 Gibberellin-response GARE-motif, P-box
MYBHv1结合位点 MYBHv1 binding site CCAAT-box
涉及光响应的MYBHv1结合位点 MYB binding site involved in light response MRE
转录启动约-30的核心启动子 Core promoter element around -30 of transcription start TATA-box
低温响应 Low-temperature response LTR
干旱诱导 Drought induced response MBS
水杨酸(SA)反应 Salicylic acid response TCA-element
MeJA茉莉酸响应 MeJA-response CGTCA-motif, TGACG-motif
生长素(IAA)应答 Auxin-response TGA-element

Fig. 6

Expression analysis of BoGSTL21 in different organs"

Fig. 7

GUS staining analysis a-c: different stages of seed development; d, e: different stages of seedling development; f: different stages of leaf development; g-i: different stages of flower development; j, k: different stages of fruit pod development."

Fig. 8

Expression analysis of BoGSTL21 in stigma past pollination under bots self and cross pollination conditions SP: self-pollination; CP: cross-pollination."

Table 3

Functional annotation analysis of candidate proteins"

候选蛋白Candidate protein 蛋白名称
Protein name
Functional annotations
BoFAB1C 1-磷脂酰肌醇-3-磷酸5-激酶
phosphate 5-kinase
具有1-磷脂酰肌醇-3-磷酸5-激酶活性, ATP结合,参与磷脂酰肌醇磷酸化, 花粉发育, 气孔关闭的生物过程。
It has 1-phosphatidylinositol-3-phosphate 5-kinase activity, ATP binding, participates in the biological processes of phosphatidylinositol phosphorylation, pollen development, and stomatal closure.
BoPATL2 patellin-2 PATL属于具有高尔基动力学(GOLD)结构域和Sec14p-like结构域串联的蛋白质家族。PATL受生长素调节。
PATL belongs to a family of proteins with a Golgi dynamics (GOLD) domain and a Sec14p-like domain tandem. PATL is regulated by auxin.
BoF9N12_9 磷酸核糖3-差向异构酶
Ribulose-phosphate 3-epimerase
属于醛缩酶型TIM桶家族蛋白, 参与碳水化合物代谢过程, 磷酸戊糖途径, 氨基酸的生物合成。
Belongs to the aldolase type TIM barrel family protein, involved in carbohydrate metabolism, pentose phosphate pathway, amino acid biosynthesis.

Table 4

Interaction analysis of plasmid co-transformation yeast"

Yeast strain (plasmid)
Yeast medium
1 Y2HGold (pGADT7-T×pGBKT7-53) SD/-Leu/-Trp 是Yes 白色White
2 Y2HGold (pGADT7-T×pGBKT7-Lam) SD/-Leu/-Trp 是Yes 红色Red
3 Y2HGold (pGADT7-BoFAB1C×pGBKT7-BoGSTL21) SD/-Leu/-Trp 是Yes 白色White
4 Y2HGold (pGADT7-BoPATL2×pGBKT7-BoGSTL21) SD/-Leu/-Trp 是Yes 白色White
5 Y2HGold (pGADT7-BoF9N12×pGBKT7-BoGSTL21) SD/-Leu/-Trp 是Yes 白色White
6 Y2HGold (pGADT7-T×pGBKT7-53) SD/-Ade/-His/-Leu/-Trp 是Yes 白色White
7 Y2HGold (pGADT7-T×pGBKT7-Lam) SD/-Ade/-His/-Leu/-Trp 是Yes 无色No
8 Y2HGold (pGADT7-BoFAB1C×pGBKT7-BoGSTL21) SD/-Ade/-His/-Leu/-Trp 是Yes 白色White
9 Y2HGold (pGADT7-BoPATL2×pGBKT7-BoGSTL21) SD/-Ade/-His/-Leu/-Trp 是Yes 白色White
10 Y2HGold (pGADT7-BoF9N12×pGBKT7-BoGSTL21) SD/-Ade/-His/-Leu/-Trp 是Yes 白色White

Fig. 9

Interaction of BoFAB1C/BoGSTL21, BoPATL2/BoGSTL 21, and BoF9N12_9/BoGSTL21 in yeast two-hybrid assay The first to third row indicates pGADT7-BoFAB1C/BoPATL2/ BoF9N12_9×pGBDT7-BoGSTL21; the fourth row indicates positive control (pGADT7-T×pGBDT7-p53); the fifth row indicates negative control (pGADT7-T×pGBDT7-Lam). DDO: SD/-Leu/-Trp; QDO: SD/-Leu/-Trp/-His/-Ade/."

Fig. 10

Prokaryotic expression of BoGSTL21 protein M: molecular weight standard of protein; 1: BoGSTL21-pGEX- 4T-1 is an uninduced control; 2: BoGSTL21-pGEX-4T-1 is the purified fusion protein; 3: pGEX-4T-1 protein; 4: BoGSTL21- pGEX-4T-1 purified protein."

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