Skip to main content
SpringerLink
Log in

In planta characterization of a tau class glutathione S-transferase gene from Juglans regia (JrGSTTau1) involved in chilling tolerance

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

JrGSTTau1 is an important candidate gene for plant chilling tolerance regulation.

Abstract

A tau subfamily glutathione S-transferase (GST) gene from Juglans regia (JrGSTTau1, GeneBank No.: KT351091) was cloned and functionally characterized. JrGSTTau1 was induced by 16, 12, 10, 8, and 6 °C stresses. The transiently transformed J. regia showed much greater GST, glutathione peroxidase (GPX), superoxide dismutase (SOD), and peroxidase (POD) activities and lower H2O2, malondialdehyde (MDA), reactive oxygen species (ROS), and electrolyte leakage (EL) rate than prokII (empty vector control) and RNAi::JrGSTTau1 under cold stress, indicating that JrGSTTau1 may be involved in chilling tolerance. To further confirm the role of JrGSTTau1, JrGSTTau1 was heterologously expressed in tobacco, transgenic Line5, Line9, and Line12 were chosen for analysis. The germinations of WT, Line5, Line9, and Line12 were similar, but the fresh weight, primary root length, and total chlorophyll content (tcc) of the transgenic lines were significantly higher than those of WT under cold stress. When cultivated in soil, the GST and SOD activities of transgenic tobacco were significantly higher than those of WT; however, the MDA and H2O2 contents of WT were on average 1.47- and 1.96-fold higher than those of Line5, Line9, and Line12 under 16 °C. The DAB, Evans blue, and PI staining further confirmed these results. Furthermore, the abundances of NtGST, MnSOD, NtMAPK9, and CDPK15 were elevated in 35S::JrGSTTau1 tobacco compared with WT. These results suggested that JrGSTTau1 improves the plant chilling tolerance involved in protecting enzymes, ROS scavenging, and stress-related genes, indicating that JrGSTTau1 is a candidate gene for the potential application in molecular breeding to enhance plant abiotic stress tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abdallah IB, Tlili N, Martinez-Force E, Rubio AG, Perez-Camino MC, Albouchi A, Boukhchina S (2015) Content of carotenoids, tocopherols, sterols, triterpenic and aliphatic alcohols, and volatile compounds in six walnuts (Juglans regia L.) varieties. Food Chem 173:972–978

    Article  CAS  PubMed  Google Scholar 

  • Benekos K, Kissoudis C, Nianiou-Obeidat I, Labrou N, Madesis P, Kalamaki M, Makris A, Tsaftaris A (2010) Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J Biotechnol 150:195–201

    Article  CAS  PubMed  Google Scholar 

  • Chan C (2014) Lam HM A putative lambda class glutathione S-transferase enhances plant survival under salinity stress. Plant Cell Physiol 55:570–579

    Article  CAS  PubMed  Google Scholar 

  • Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chronopoulou E, Madesis P, Tsaftaris A, Labrou NE (2014) Cloning and characterization of a biotic-stress-inducible glutathione transferase from Phaseolus vulgaris. Appl Biochem Biotechnol 172:595–609

    Article  CAS  PubMed  Google Scholar 

  • Cui L, Huang Q, Yan B, Wang Y, Qian Z, Pan J, Kai G (2015) Molecular cloning and expression analysis of a Cu/Zn SOD gene (BcCSD1) from Brassica campestris ssp. chinensis. Food Chem 186:306–311

    Article  CAS  PubMed  Google Scholar 

  • Dixit P, Mukherjee PK, Ramachandran V, Eapen S (2011) Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6:0016360

    Article  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:1–10

    Article  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254

    Article  CAS  PubMed  Google Scholar 

  • George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin-induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genom 11:73

    Article  Google Scholar 

  • Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Ahn IY, Cheon J, Park H (2009) Molecular cloning and thermal stress-induced expression of a pi-class glutathione S-transferase (GST) in the Antarctic bivalve Laternula elliptica. Comp Biochem Physiol 152:207–213

    Article  Google Scholar 

  • Kim YJ, Lee OR, Lee S, Kim KT, Yang DC (2012) Isolation and characterization of a theta glutathione S-transferase gene from Panax ginseng Meyer. J Ginseng Res 36:449–460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kouno T, Ezaki B (2013) Multiple regulation of Arabidopsis AtGST11 gene expression by four transcription factors under abiotic stresses. Physiol Plant 148:97–104

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Expression of a rice Lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazard Mater 248:228–237

    Article  PubMed  Google Scholar 

  • Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu D, Liu Y, Rao J, Wang G, Li H, Ge F, Chen C (2013) Overexpression of the glutathione S-transferase gene from Pyrus pyrifolia fruit improves tolerance to abiotic stress in transgenic tobacco plants. Mol Biol 47:591–601

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lo Piero AR, Mercurio V, Puglisi I, Petrone G (2009) Gene isolation and expression analysis of two distinct sweet orange [Citrus sinensis L. (Osbeck)] tau-type glutathione transferases. Gene 443:143–150

    Article  CAS  PubMed  Google Scholar 

  • Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitam Horm 72:155–202

    Article  CAS  PubMed  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23:80–92

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sharma R, Sahoo A, Devendran R, Jain M (2014) Over-expression of a rice tau class glutathione s-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PLoS One 9:e92900

    Article  PubMed Central  PubMed  Google Scholar 

  • Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900–1902

    Article  CAS  PubMed  Google Scholar 

  • Skopelitou K, Muleta AW, Papageorgiou AC, Chronopoulou E, Labrou NE (2015) Catalytic features and crystal structure of a tau class glutathione transferase from Glycine max specifically upregulated in response to soybean mosaic virus infections. Biochim Biophys Acta 2:166–177

    Article  Google Scholar 

  • Wang Z, Huang S, Jia C, Liu J, Zhang J, Xu B, Jin Z (2013) Molecular cloning and expression of five glutathione S-transferase (GST) genes from Banana (Musa acuminata L. AAA group, cv. Cavendish). Plant Cell Rep 32:1373–1380

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Tian YS, Xing XJ, Peng RH, Zhu B, Gao JJ, Yao QH (2015a) Over-expression of AtGSTU19 provides tolerance to salt, drought and methyl viologen stresses in Arabidopsis. Physiol Plant 14:12347

    Google Scholar 

  • Xu F, Deng G, Cheng S, Zhang W, Huang X, Li L, Cheng H, Rong X, Li J (2012) Molecular cloning, characterization and expression of the phenylalanine ammonia-lyase gene from Juglans regia. Molecules 17:7810–7823

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Xing XJ, Tian YS, Peng RH, Xue Y, Zhao W, Yao QH (2015b) Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS One 10:e0136960

    Article  PubMed Central  PubMed  Google Scholar 

  • Yan H, Jia H, Gao H, Guo X, Xu B (2013) Identification, genomic organization, and oxidative stress response of a sigma class glutathione S-transferase gene (AccGSTS1) in the honey bee, Apis cerana cerana. Cell Stress Chaperones 18:415–426

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang G, Wang Y, Xia D, Gao C, Wang C, Yang C (2014) Overexpression of a GST gene (ThGSTZ1) from Tamarix hispida improves drought and salinity tolerance by enhancing the ability to scavenge reactive oxygen species. Plant Cell Tiss Org 117:99–112

    Article  CAS  Google Scholar 

  • Zhang X, Wang L, Meng H, Wen H, Fan Y (2011) Zhao J Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao J, Zhang S, Yang T, Zeng Z, Huang Z, Liu Q, Wang X, Leach J, Leung H, Liu B (2015) Global transcriptional profiling of a cold-tolerant rice variety under moderate cold stress reveals different cold stress response mechanisms. Physiol Plant 154:381–394

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Liu G, Meng X, Li Y, Wang Y (2012) A versatile Agrobacterium-mediated transient gene expression system for herbaceous plants and trees. Biochem Genet 50:761–769

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The current study was supported by grants from the Agricultural Science and Technology Entrepreneurship and Research Program of Shaanxi Province (2015NY122), the Faculty Inaugurating Program of Northwest A & F University (2014BSJJ038, QN2013080, 2452015171); and the Science and Technology Central Innovation Projects of Shaanxi Province (2012KTZB02-01-01).

Author information

Authors and Affiliations

  1. Laboratory of Walnut Research Center, College of Forestry, Northwest A & F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Guiyan Yang, Shaobing Peng, Yudong Sun, Caixia Jia & Meizhi Zhai

  2. College of Life Science and Technology, Central South University of Forestry and Technology, 498 Shaoshan South Road, Changsha, 410004, Hunan Province, People’s Republic of China

    Zhenggang Xu

Authors
  1. Guiyan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenggang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shaobing Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yudong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Caixia Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meizhi Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Meizhi Zhai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by L. Peña.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 476 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, G., Xu, Z., Peng, S. et al. In planta characterization of a tau class glutathione S-transferase gene from Juglans regia (JrGSTTau1) involved in chilling tolerance. Plant Cell Rep 35, 681–692 (2016). https://doi.org/10.1007/s00299-015-1912-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1912-8

Keywords

Search

Navigation