Abstract
Genes encoding glutathione S-transferases (GSTs) are potential targets for creating stress-tolerant plants by genetic engineering techniques. Despite the partial duplication of the functions of GST genes in the plant organism, each gene can perform a specific role in the regulation of growth under changing environmental conditions. Therefore it is important to investigate the functions of individual GST genes. The purpose of our study was to assess the role of the AtGSTF11 gene of Arabidopsis thaliana on the growth regulation and stress tolerance of transgenic plants. We have identified that the expression of the AtGSTF11 gene in A. thaliana is induced by salinity and drought. Constitutive expression of the AtGSTF11 gene in transgenic Nicotiana tabacum plants contributed to the improvement of root growth under salinity and cold treatment. Under normal and drought stress conditions overexpression of the AtGSTF11 promoted the shoot growth of tobacco. In the transgenic plants, drought stress also induced an increase of proline content and activity of superoxide dismutase and catalase, which are biochemical markers of stress tolerance. We discussed that the AtGSTF11 gene is a potential target for direct changes in the productivity and abiotic stress tolerance of plants by genetic engineering techniques.
REFERENCES
Nianiou-Obeidat, I., Madesis, P., Kissoudis, C., Voulgari, G., Chronopoulou, E., Tsaftaris, A., and Labrou, N.E., Plant glutathione transferase-mediated stress tolerance: functions and biotechnological applications, Plant Cell Rep., 2017, vol. 36, no. 6, p. 791. https://doi.org/10.1007/s00299-017-2139-7
Kalinina, E.V., Chernov, N.N., and Novichkova, M.D., Role of glutathione, glutathione transferase, and glutaredoxin in regulation of redox-dependent processes, Biochemistry (Moscow), 2014, vol. 79, no. 13, p. 1562. https://doi.org/10.1134/S0006297914130082
Salinas, A.E. and Wong, M.G., Glutathione S-transferases, Curr. Med. Chem., 1999, vol. 6, p. 279.
Islam, S, Rahman, I.A, Islam, T., and Ghosh, A., Genome-wide identification and expression analysis of glutathione S-transferase gene family in tomato: Gaining an insight to their physiological and stress-specific roles, PLoS One, 2017, vol. 2, p. e0187504. https://doi.org/10.1371/journal.pone.0187504
Sharma, R., Sahoo, A., Devendran, R., and Jain, M., Over-expression of a rice tau class glutathione S-transferases gene improves tolerance to salinity and oxidative stresses in Arabidopsis, PLoS One, 2014, vol. 9, p. e92900. https://doi.org/10.1371/journal.pone.0092900
Takesawa, T., Ito, M., Kanazaki, H., Kameya, N., and Nakamuro, I., Over-expression of ζ glutathione S-transferase in transgenic rice enhances germination and growth at low temperature, Mol. Breed, 2002, vol. 9, p. 93. https://doi.org/10.1023/A:1026718308155
Roxas, V.P., Smith, R.K., Allen, E.R., and Allen, R.D., Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress, Nat. Biotechnol., 1997, vol. 15, p. 988. https://doi.org/10.1038/nbt1097-988
Fragoulaki, M.N., Axarli, I.A., Labrou, N.E., and Clonis, Y.D., Recombinant glutathione S-transferase for the determination of the herbicide alachlor: The foundations of an optical biosensor, 1st UK-US Conference on Chemical and Biological Sensors and Detectors, London, 2007.
Zhao, F.Y., Liu, T., and Xu, Z.J., Modified responses of root growth and reactive oxygen species-scavenging system to combined salt and heat stress in transgenic rice, Russ. J. Plant Physiol., 2010, vol. 57, p. 518. https://doi.org/10.1134/S1021443710040096
Liu, L., Liu, Y., Rao, J., Wang, G., Li, H., Ge, F., and Chen C., Overexpression of the glutathione S-transferase gene from Pyrus pyrifolia fruit improves tolerance to abiotic stress in transgenic tobacco plants, Mol. Biol., 2013, vol. 47, p. 515. https://doi.org/10.1134/S0026893313040109
Dong, Y., Li, C., Zhang, Y., He, Q., Daud, M.K., Chen, J., and Zhu, S., Glutathione S-transferase gene family in Gossypium raimondii and G. arboreum: Comparative genomic study and their expression under salt stress, Front. Plant Sci., 2016, vol. 7, p. 139. https://doi.org/10.3389/fpls.2016.00139
Chen, J.H., Jiang, H.W., Hsieh, E.J., Chen, H.Y., Chien, C.T., Hsieh, H.L., and Lin, T.P., 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., 2012, vol. 158, no. 1, p. 340. https://doi.org/10.1104/pp.111.181875
Musin, Kh.G., Fedyaev, V.V., and Kuluev, B.R., State of antioxidant system and long-term storage of tobacco hairy roots with constitutive expression of glutathione-S-transferase gene AtGSTF11, Russ. J. Plant Physiol., 2021, vol. 68, p. 641. https://doi.org/10.1134/S1021443721040105
Mikhaylova, E., Khusnutdinov, E., Shein, M.Y., Alekseev, V.Y., Nikonorov, Y., and Kuluev, B., The role of the GSTF11 gene in resistance to powdery mildew infection and cold stress, Plants, 2021, vol. 10, p. 2729. https://doi.org/10.3390/plants10122729
Kuluev, B, Mikhaylova, E., Ermoshin, A., Veselova, S., Tugbaeva, A., Gumerova, G., Gainullina, K., and Zaikina, E., The ARGOS-LIKE genes of Arabidopsis and tobacco as targets for improving plant productivity and stress tolerance, J. Plant Physiol., 2019, vol. 242, p. 153033. https://doi.org/10.1016/j.jplph.2019.153033
Xin, X.F., Nomura, K., Underwood, W., and He, S.Y., Induction and suppression of PEN3 focal accumulation during Pseudomonas syringae pv. tomato DC3000 infection of Arabidopsis, Mol. Plant Microbe Interact., 2013, vol. 26, no. 8, p. 861. https://doi.org/10.1094/MPMI-11-12-0262-R
Kuluev, B.R., Avalbaev, A.M., Mikhaylova, E.V., Nikonorov, Y.M., Berezhneva, Z.A., and Chemeris, A.V., Expression profiles and hormonal regulation of tobacco expansin genes and their involvement in abiotic stress response, J. Plant Physiol., 2016, vol. 206, p. 1. https://doi.org/10.1016/j.jplph.2016.09.001
Kuluev, B.R., Mikhaylova, E.V., Berezhneva, Z.A., Nikonorov, Y.M., Postrigan, B.N., Kudoyarova, G.R., and Chemeris, A.V., Expression profiles and hormonal regulation of tobacco NtEXGT gene and its involvement in abiotic stress response, Plant Physiol. Biochem., 2017, vol. 111, p. 203. https://doi.org/10.1016/j.plaphy.2016.12.005
Schmidt, G.W. and Delaney, S.K., Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress, Mol. Genet. Genomics, 2010, vol. 283, p. 233. https://doi.org/10.1007/s00438-010-0511-1
Beauchamp, C. and Fridovich, L., Superoxide dismutase: improved assays and an assay applicable to acrylamide gels, Anal. Biochem., 1971, vol. 44, p. 276.
Goth, L., A simple method for determination of serum catalase activity and revision of reference range, Clin. Chim. Acta, 1991, vol. 196, nos. 2–3, p. 143.
Bates, L.S., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, p. 205.
Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, p. 248.
Kolupaev, Yu.E., Plant cell antioxidants and their role in ROS signaling and plant resistance, Usp. Sovrem. Biol., 2016, vol. 136, p. 181.
Abdul Kayum, M., Nath, U.K., Park, J.I., Biswas, M.K., Choi, E.K., Song, J.Y., Kim, H.T., and Nou, I.S., Genome-wide identification, characterization, and expression profiling of glutathione S-transferase (GST) family in pumpkin reveals likely role in cold-stress tolerance, Genes (Basel), 2018, vol. 9, no. 2, p. E84. https://doi.org/10.3390/genes9020084
Xu, J., Xing, X.J., Tian, Y.S., Peng, R.H., Xue, Y., Zhao, W., and Yao, Q.-H., Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress, PLoS One, 2015, vol. 10, no. 9, p. e0136960. https://doi.org/10.1371/journal.pone.0136960
Vijayakumar, H., Thamilarasan, S.K., Shanmugam, A., Natarajan, S., Jung, H.J., Park, J.I., Kim, H., Chung, M.Y., and Nou, I.S., Glutathione transferases superfamily: cold-inducible expression of distinct GST genes in Brassica oleracea, Int. J. Mol. Sci., 2016, vol. 17, no. 8, p. E1211. https://doi.org/10.3390/ijms17081211
Dubey, S., Misra, P., Dwivedi, S., Chatterjee, S., Bag, S.K., Mantri, S., Asif, M.H., Rai, A., Kumar, S., Shri, M., Tripathi, P., Tripathi, R.D., Trivedi, P.K., Chakrabarty, D., and Tuli, R., Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress, BMC Genomics, 2010, vol. 11, p. 648. https://doi.org/10.1186/1471-2164-11-648
Gong, H., Jiao, Y., Hu, W.W., and Pua, E.C., Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro, Plant Mol. Biol., 2005, vol. 57, no. 1, p. 53. https://doi.org/10.1007/s11103-004-4516-1
Funding
The work supported by state assignment (project no. 122030200143-8) and grant of the President of the Russian Federation (project no. MD-2304.2020.4).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
Kuluev, B.R., Ermoshin, A.A. & Mikhaylova, E.V. Overexpression of the Glutathione S-Transferase ATGSTF11 Gene Improves Growth and Abiotic Stress Tolerance of Tobacco Transgenic Plants. Russ J Plant Physiol 69, 148 (2022). https://doi.org/10.1134/S1021443722601653
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1134/S1021443722601653