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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (10): 2665-2676.doi: 10.3724/SP.J.1006.2023.34020

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Interaction of sugarcane glutathione S-transferase ScGSTF1 with P3N-PIPO in response to SCMV infection

YANG Zong-Tao(), JIAO Wen-Di, ZHANG Hai, ZHANG Ke-Ming, CHENG Guang-Yuan, LUO Ting-Xu, ZENG Kang, ZHOU Ying-Shuan, XU Jing-Sheng()   

  1. Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University / National Engineering Research Center for Sugarcane, Fuzhou 350002, Fujian, China
  • Received:2023-01-30 Accepted:2023-04-17 Online:2023-10-12 Published:2023-04-27
  • Contact: E-mail: xujingsheng@126.com
  • Supported by:
    National Natural Science Foundation of China(31971991);Science and Technology Innovation Project of Fujian Agriculture and Forestry University(CXZX2019132G);Open Project of Guangxi Key Laboratory of Sugarcane Biology(GXKLSCB-202003)

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Abstract:

The Glutathione S-transferases (GSTs) are widely distributed in cellular organisms and participate in the regulation of growth and development, detoxification of xenobiotics, and response to stress in plants. In the present study, we screened a sugarcane (Saccharum spp. hybrid) cDNA library and obtained a GST gene from sugarcane original cultivar Badila using Sugarcane mosaic virus (SCMV)-encoded protein P3N-PIPO as bait. The open reading frame (ORF) of the cloned GST gene was 645 bp in length, encoding a protein with 214 amino acids. Sequence alignment and phylogenetic tree showed that this GST belonged to the Phi (F) class (GSTF) designated as ScGSTF1 in GST family. Further bioinformatics revealed that ScGSTF1 protein was a stable hydrophilic lipoprotein without transmembrane domain. Phylogenetic tree demonstrated that ScGSTF1 was divergent between monocotyledons and dicotyledonous, as well as in C3 and C4 plants. Yeast two-hybrid (Y2H) and biomolecular fluorescence complementation (BiFC) assays confirmed the interaction of ScGSTF1 with SCMV-P3N-PIPO. Subcellular localization assays indicated that ScGSTF1 was localized in the endoplasmic reticulum. The qRT-PCR analysis showed that ScGSTF1 gene was significantly differently expressed in different tissues of sugarcane plants with the highest expression level in the 3rd internode and the lowest expression level in leaf roll or roots. SCMV infection affected the relative expression level of ScGSTF1 gene, which was up-regulated at the early stage of infection and down-regulated later, but still maintained a significantly higher level than the control.

Key words: sugarcane, Sugarcane mosaic virus, glutathione S-transferase, P3N-PIPO, protein interaction

Table 1

Primers used in this study"

引物名称
Primer name		 引物序列
Primer sequence (5′-3′)		 策略
Strategy
pPR3-ScGSTF1-F GCAGAGTGGCCATTACGATGGCCGGCGGTGGCGGCGA 酵母双杂交载体构建
pPR3-ScGSTF1-R ATTCTCGAGAGGCCGAGCTGATGGCTTCATCATGG Vector generation for Y2H
221-ScGSTF1-F GGGGACAAGTTTGTACAAAAAAGCAGGCTTCATGGCCGGCGGTGGCGGCGA 双分子荧光互补载体构建
221-ScGSTF1-R GGGGACCACTTTGTACAAGAAAGCTGGGTCAGCTGATGGCTTCATCATGG Vector generation for BiFC
ScGSTF1-qF TGGACGAGGCGAACGAGACC 定量PCR
ScGSTF1-qR AGCGGCGGTGAGGCAGAC Real-time-qPCR
GAPDH-F CACGGCCACTGGAAGCA 内参基因[69]
GAPDH-R TCCTCAG GGTTCCTGATGCC Real-time-qPCR[69]
Actin-F CCTGAAGATCACCCTGTGCT 内参基因[70]
Actin-R GCAGTCTCCAGCTCCTGTTC Reference gene[70]
SCMV-CP-F TACAGAGAGACACACAGCTG SCMV检测[71]
SCMV-CP-R ACGCTACACCAGAAGACACT Detection of SCMV[71]

Fig. 1

Phylogenetic tree of ScGST and GST proteins from Arabidopsis and rice ScGST is highlighted in red color. The pink clade indicates Tau (GSTU), the green clade indicates dehydroascorbate reductase (DHAR), the blue clade indicates Lambda (GSTL), the red clade indicates Zeta (GSTZ), the green clade indicates tetrachlorohydroquinone dehalogenase (TCHQD), the brown clade indicates Theta (GSTT), the cyan clade indicates γ-subunit of translation elongation factor (EF1G), and the black clade indicates Phi (GSTF)."

Fig. 2

Phylogenetic tree of ScGSTF1 and GSTFs proteins from other plant species Saccharum officinarum: ScGSTF1 (OQ333021); Sorghum bicolor: SbGSTF1 (XP_002458541.1); Zea mays: ZmGSTF2 (ACG25283.1); Panicum virgatum: PvGSTF1 (XP_039849196.1); Setaria viridis: SvGSTF1 (XP034596925.1); Brachypodium distachyon: BdGSTF1 (XP_010232378.1); Hordeum vulgare: HvGSTF1 (XP_044977142.1); Triticum aestivum: TaGSTF1 (XP_044350191.1); Nicotiana tabacum: NbGSTF1 (XP_016472830.1); Solanum tuberosum: StGSTF1 (KAH0657425.1); Arabidopsis thaliana: AtGSTF13 (AT3G62760); Glycine max: GmGSTF21 (NP_001291446.1); Vitis vinifera: VvGSTF13 (RVW54521.1); Prunus persica: PpGSTF13 (XP_007209587.1); Populus trichocarpa: PtGSTF13 (XP_006386755.1). The red box, the green box, and the yellow box indicate the subgroup I-1, the subgroup I-2, and the group II, respectively."

Fig. 3

Secondary structures of ScGSTF1 and GSTFs from other plant species Saccharum officinarum: ScGSTF1 (OQ333021); Arabidopsis thaliana: AtGSTF13 (AT3G62760); Populus trichocarpa: PtGSTF1 (Potri.002G015100.1); Oryza sativa: OsGSTF1 (XP_015642391.1). Secondary structures are labeled and shown using gray arrows (β-strands) and blue squiggles (α-helices)."

Fig. 4

Subcellular localization of ScGSTF1 fused with YFP in the epidermal cells of N. benthamiana Subcellular localization of ScGSTF1-YFP. Bar: 25 μm."

Fig. 5

Protein-protein interactions between ScGSTF1 and SCMV-P3N-PIPO Y2H assay The positive and negative controls are yeast cotransformants with pNubG-Fe65 plus pTSU2-APP and pNubG-Fe65 plus pPR3-N, respectively. DDO+X-Gal: synthetic defined yeast minimal medium lacking Leu and Trp but plus the 5-Bromo-4-Chloro-3-Indolyl β-D-Galactopyranoside (X-Gal); QDO+X-Gal: synthetic defined yeast minimal medium lacking Leu, Trp, His, and Ade but plus the X-Gal."

Fig. 6

Protein-protein interaction between ScGSTF1 and SCMV-P3N-PIPO by BiFC assays A: the C-terminal half of YFP was fused to the N-terminal of SCMV-P3N-PIPO to generate P3N-PIPO-YC, while the N-terminal half of YFP was fused to the C-terminal of ScGSTF1 to generate ScGSTF1-YN. B: the C-terminal half of YFP was fused to the N-terminal of ScGSTF1 to generate ScGSTF1-YC, while the N-terminal half of YFP was fused to the C-terminal of SCMV-P3N-PIPO to generate P3N-PIPO-YN. Plasmids combination of P3N-PIPO-YC plus ScGSTF1-YN (A), ScGSTF1-YC plus SCMV-P3N-PIPO-YN (B) were individually co-injected into N. benthamiana leaves for transient expression. The fluorescent signal was monitored by confocal microscopy at 48 h post infiltration. Bar: 25 μm."

Fig. 7

Tissue specific expression analysis of ScGSTF1 gene LR: leaf roll; +1 L: the first leaf; +7 L: the 7th leaf; +3 I: the 3rd internode; +8 I: the 8th internode; R: root. The error bar represents the standard error of each treating group (n = 3). Bars superscripted by different lowercase letters are significantly different at P < 0.05."

Fig. 8

Relative expression profile of ScGSTF1 gene under the infection of SCMV The error bar represents the standard error of each treatment group (n = 3). Bars superscripted by different lowercase letters are significantly different at P < 0.05."

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