Molecular cloning, identification of GSTs family in sunflower and their regulatory roles in biotic and abiotic stress

  • Ligong Ma
  • Yunhua Zhang
  • Qinglin Meng
  • Fengmei Shi
  • Jia Liu
  • Yichu Li
Original Paper


Glutathione-S-transferase (GST) genes exist widely in plants and play major role in metabolic detoxification of exogenous chemical substances and oxidative stress. In this study, 14 sunflower GST genes (HaGSTs) were identified based on the sunflower transcriptome database that we had constructed. Full-length cDNA of 14 HaGTSs were isolated from total RNA by reverse transcription PCR (RT-PCR). Sunflower was received biotic stress (Sclerotinia sclerotiorum) and abiotic stress (NaCl, low-temperature, drought and wound). GST activity was measured by using the universal substrate. The results showed that most of the HaGSTs were up-regulated after NaCl and PEG6000-induced stresses, while a few HaGSTs were up-regulated after S. sclerotiorum, hypothermia and wound-induced stressed, and there was correlation between the changes of GST activity and the expression of HaGSTs, indicating that HaGSTs may play regulatory role in the biotic and abiotic stress responses. 14 HaGSTs from sunflower were identified, and the expression of HaGSTs were tissue-specific and played regulatory roles in both stress and abiotic stress.


Glutathione-S-transferase Sunflower HaGSTs Biotic stress Abiotic stress Oxidative stress 



Thanks to Dr. Chen Jishan and Dr. Ma Jun from Heilongjiang Academy of Agricultural Sciences for their help in data analysis.


This word sponsored by Project of National Specialty Oil Industry Technology System (Grant Number CARS-14-1-20) and Postdoctoral Research Fund of Heilongjiang Academy of Agricultural Sciences (Grant Number LRB 185216).

Compliance with ethical standards

Conflict of interest

The authors declare there have no conflict of interest.

Ethics approval

This study was approved by The Ethics Committee of Institute of Plant Protection, Heilongjiang Academy of Agricultural Sciences.

Informed consent

Participants have provided their written informed consent to participate in this study.

Supplementary material

11274_2018_2481_MOESM1_ESM.doc (118 kb)
Supplementary material 1 (DOC 118 KB)
11274_2018_2481_MOESM2_ESM.docx (20 kb)
Supplementary material 2 (DOCX 21 KB)


  1. An J, Yang P, Cao Y, Geng J, Ren P, You Z, Wang Y, Zhang Z, Yang J (2017) Cloning and expression analysis of a novel glutathione-S-transferase gene, MsGST, from alfalfa (Medicago sativa). Indian J Genet Plant Breed 77(3):394CrossRefGoogle Scholar
  2. Badouin H, Gouzy J, Grassa CJ, Murat F, Staton SE, Cottret L, Lelandaisbrière C, Owens GL, Carrère S, Mayjonade B (2017) The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546(7656):148CrossRefPubMedGoogle Scholar
  3. Basantani M, Srivastava A (2007) Plant glutathione transferases—a decade falls short. Can J Bot 85(5):443–456CrossRefGoogle Scholar
  4. Chi Y, Cheng Y, Vanitha J, Kumar N, Ramamoorthy R, Ramachandran S, Jiang S-Y (2010) Expansion mechanisms and functional divergence of the glutathione S-transferase family in sorghum and other higher plants. DNA Res 18(1):1–16CrossRefPubMedPubMedCentralGoogle Scholar
  5. Choi YI, Noh EW, Kim HJ, Shim D (2013) Overexpression of poplar GSTU51 confers selective tolerance to both mercury and methyl viologen but not to CDNB or cadmium in transgenic poplars. Plant Biotechnol Rep 7(2):175–184CrossRefGoogle Scholar
  6. Chronopoulou E, Georgakis N, Nianiou-Obeidat I, Madesis P, Perperopoulou F, Pouliou F, Vasilopoulou E, Ioannou E, Ataya F, Labrou N (2017) Plant glutathione transferases in abiotic stress response and herbicide resistance. In: Glutathione in plant growth, development, and stress tolerance. Springer, Cham, pp. 215–233CrossRefGoogle Scholar
  7. Csiszár J, Váry Z, Horváth E, Gallé Á, Tari I (2011) Role of glutathione transferases in the improved acclimation to salt stress in salicylic acid-hardened tomato. Acta Biol Szeged 55(1):67–68Google Scholar
  8. Czarnocka W, Karpiński S (2018) Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radical Biol Med. CrossRefGoogle Scholar
  9. Ding N, Wang A, Zhang X, Wu Y, Wang R, Cui H, Huang R, Luo Y (2017) Identification and analysis of glutathione S-transferase gene family in sweet potato reveal divergent GST -mediated networks in aboveground and underground tissues in response to abiotic stresses. BMC Plant Biol 17(1):225CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dixon DP, Cole DJ, Edwards R (1998) Purification, regulation and cloning of a glutathione transferase (GST) from maize resembling the auxin-inducible type-III GSTs. Plant Mol Biol 36(1):75CrossRefPubMedGoogle Scholar
  11. Dixon DP, Lapthorn A, Edwards R (2005) Plant glutathione transferases. Genome Biol 401(3):169–186Google Scholar
  12. Dowd C, Wilson IW, Mcfadden H (2004) Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol Plant Microbe Interact 17(6):654–667CrossRefPubMedGoogle Scholar
  13. Gong H, Hu WW, Jiao Y, Pua EC (2005) Molecular characterization of a Phi-class mustard (Brassica juncea) glutathione S-transferase gene in Arabidopsis thaliana by 5′-deletion analysis of its promoter. Plant Cell Rep 24(7):439–447CrossRefPubMedGoogle Scholar
  14. Habig WHJW. (1981) Assay for differentiation of GST. Method Enzymol 77:735–740Google Scholar
  15. Han Q, Chen R, Yang Y, Cui X, Ge F, Chen C, Liu D (2016) A glutathione S-transferase gene from Lilium regale Wilson confers transgenic tobacco resistance to Fusarium oxysporum. Sci Hortic 198:370–378CrossRefGoogle Scholar
  16. Han XM, Yang ZL, Liu YJ, Yang HL, Zeng QY (2018) Genome-wide profiling of expression and biochemical functions of the Medicago, glutathione S-transferase gene family. Plant Physiol Biochem 126:126–133CrossRefPubMedGoogle Scholar
  17. Hewezi T, Léger M, Gentzbittel L (2008) A comprehensive analysis of the combined effects of high light and high temperature stresses on gene expression in sunflower. Ann Bot 102(1):127–140CrossRefPubMedPubMedCentralGoogle Scholar
  18. Islam M, Chowdhury A, Rahman M, Rohman M (2015) Comparative investigation of glutathione S-transferase (GST) in different crops and purification of high active GSTs from Onion (Allium cepa L.). J Plant Sci 3:162–170Google Scholar
  19. Islam S, Rahman IA, Islam T, Ghosh A (2017) 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 12(11):e0187504CrossRefPubMedPubMedCentralGoogle Scholar
  20. Islam S, Choudhury M, Majlish AK, Islam T, Ghosh A (2018) Comprehensive genome-wide analysis of glutathione S-transferase gene family in potato (Solanum tuberosum) and their expression profiling in various anatomical tissues and perturbation conditions. Gene 639:149–162CrossRefPubMedGoogle Scholar
  21. 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(7):4823–4832CrossRefPubMedGoogle Scholar
  22. Kumar SAM, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Expression of a rice lambda class of glutathione S-transferase, Os GSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazard Mater 248:228–237CrossRefPubMedGoogle Scholar
  23. Labrou NE, Tsaftaris A, Madesis P, Nianiou-Obeidat I, Axarli I, Bosmali E, Voulgari G, Perperopoulou F, Pouliou F, Chantzikonstantinou M (2015) Plant glutathione transferases: structure, antioxidant catalytic function and in planta protective role in biotic and abiotic stress. Curr Chem Biol 8(2):58–75CrossRefGoogle Scholar
  24. Li Z, Wang Y, Chen Y, Zhang J, Fernando WGD (2009) Genetic diversity and differentiation of Sclerotinia sclerotiorum populations in sunflower. Phytoparasitica 37(1):77–85CrossRefGoogle Scholar
  25. Li-Gong MA, Meng QL, Zhang YH, Liu ZH, Wang ZY, University NF (2015) Clone and function of a glutathione-S-transferase gene from sunflower (Helianthus annuus). Chin J Oil Crop Sci 37(5):635–643Google Scholar
  26. Liu Y, Han X, Ren L, Yang H, Zeng Q (2013) Functional divergence of the glutathione S-transferase supergene family in Physcomitrella patens reveals complex patterns of large gene family evolution in land plants. Plant Physiol 161(2):773CrossRefPubMedGoogle Scholar
  27. Lo CL, Madesis P, Tsaftaris A, Lo Piero AR (2015) Tobacco plants over-expressing the sweet orange tau glutathione transferases (CsGSTUs) acquire tolerance to the diphenyl ether herbicide fluorodifen and to salt and drought stresses. Phytochemistry 116(1):69Google Scholar
  28. Lu ZX, Gaudet DA, Frick M, Puchalski B, Genswein B, Laroche A (2005) Identification and characterization of genes differentially expressed in the resistance reaction in wheat infected with Tilletia tritici, the common bunt pathogen. J Biochem Mol Biol 38(4):420–431PubMedGoogle Scholar
  29. Marimo P, Hayeshi R, Mukanganyama S, Marimo P, Hayeshi R, Mukanganyama S (2016) Inactivation of glutathione transferase 2 by Epiphyllocoumarin. Biochem Res Int 2016(6):1–8CrossRefGoogle Scholar
  30. Mayer Z, Duc N, Posta K (2017) Gene expression of glutathione-S-transferase in sunflower (Helianthus annuus L.) inoculated with arbuscular mycorrhizal fungi under temperature stressesGoogle Scholar
  31. Mcgonigle B, O’Keefe DP (2000) A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol 124(3):1105–1120CrossRefPubMedPubMedCentralGoogle Scholar
  32. Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490CrossRefPubMedGoogle Scholar
  33. Nianiou-Obeidat I, Madesis P, Kissoudis C, Voulgari G, Chronopoulou E, Tsaftaris A, Labrou NE (2017) Plant glutathione transferase-mediated stress tolerance: functions and biotechnological applications. Plant Cell Rep 36(6):1–15CrossRefGoogle Scholar
  34. Pflugmacher S, Schröder P Jr, Sandermann H (2000) Taxonomic distribution of plant glutathione S-transferases acting on xenobiotics. Phytochemistry 54(3):267CrossRefPubMedGoogle Scholar
  35. Pierre-Alexandre L, Bastiaan B, Olivier K, Arnaud H, Nicolas R (2014) The still mysterious roles of cysteine-containing glutathione transferases in plants. Front Pharmacol 5(192):1–22Google Scholar
  36. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J Cell Mol Biol 58(1):53–68CrossRefGoogle Scholar
  37. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101CrossRefPubMedGoogle Scholar
  38. Seppänen MM, Cardi T, Hyökki MB, Pehu E (2000) Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. Plant Sci 153(2):125CrossRefPubMedGoogle Scholar
  39. Soonyoung A, Seonae K, Yun HK (2016) Glutathione S-transferase genes differently expressed by pathogen-infection in Vitis flexuosa. Plant Breed Biotechnol 4(5):61–70Google Scholar
  40. Soranzo N, Sari GM, Mizzi L, De TG, Frova C (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271:511–521CrossRefPubMedGoogle Scholar
  41. Ting L, ZhiLing Y, Xue Y, YanJing L, XiaoRu W, QingYin Z (2009) Extensive functional diversification of the populus glutathione S-transferase supergene family. Plant Cell 21(12):3749CrossRefGoogle Scholar
  42. Vollenweider S, Weber H, Stolz S, Chételat A, Farmer EE (2010) Fatty acid ketodienes and fatty acid ketotrienes: michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves. Plant J 24(4):467Google Scholar
  43. Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49(5):515CrossRefPubMedGoogle Scholar
  44. Wang Z, Zhang JB, Jia CH, Liu JH, Li YQ, Yin XM, Xu BY, Jin ZQ (2012) De novo characterization of the banana root transcriptome and analysis of gene expression under Fusarium oxysporum f. sp. Cubense tropical race 4 infection. BMC Genomics 13(1):650CrossRefPubMedPubMedCentralGoogle Scholar
  45. Yan Y, Jia H, Wang F, Wang C, Liu S, Guo X (2015) Overexpression of GhWRKY27a reduces tolerance to drought stress and resistance to Rhizoctonia solani infection in transgenic Nicotiana benthamiana. Front Physiol 6(265):265PubMedPubMedCentralGoogle Scholar
  46. Yang G, Xu Z, Peng S, Sun Y, Jia C, Zhai M (2016) In planta characterization of a tau class glutathione S-transferase gene from Juglans regia (JrGSTTau1) involved in chilling tolerance. Plant Cell Rep 35(3):681–692CrossRefPubMedGoogle Scholar
  47. Zhu JH, Li HL, Guo D, Wang Y, Dai HF, Mei WL, Peng SQ (2016) Transcriptome-wide identification and expression analysis of glutathione S-transferase genes involved in flavonoids accumulation in Dracaena cambodiana. Plant Physiol Biochem 104:304–311CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Heilongjiang Academy of Agricultural Sciences Postdoctoral ProgrammeHarbinChina
  2. 2.Institute of Plant ProtectionHeilongjiang Academy of Agricultural SciencesHarbinChina

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