Abstract
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.
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The datasets generated and analyzed during the current study are not publicly available due to statutory provisions regarding data- and privacy protection, the dataset supporting the conclusions of this article is available upon reasonable request directed to the corresponding author.
References
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):394
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):148
Basantani M, Srivastava A (2007) Plant glutathione transferases—a decade falls short. Can J Bot 85(5):443–456
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):1–16
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):175–184
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. 215–233
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):67–68
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. https://doi.org/10.1016/j.freeradbiomed.2018.01.011
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):225
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):75
Dixon DP, Lapthorn A, Edwards R (2005) Plant glutathione transferases. Genome Biol 401(3):169–186
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):654–667
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):439–447
Habig WHJW. (1981) Assay for differentiation of GST. Method Enzymol 77:735–740
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 198:370–378
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 126:126–133
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):127–140
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 3:162–170
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):e0187504
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 639:149–162
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):4823–4832
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 248:228–237
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):58–75
Li Z, Wang Y, Chen Y, Zhang J, Fernando WGD (2009) Genetic diversity and differentiation of Sclerotinia sclerotiorum populations in sunflower. Phytoparasitica 37(1):77–85
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):635–643
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):773
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):69
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):420–431
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):1–8
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 stresses
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):1105–1120
Mittler R, Vanderauwera S, Gollery M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490
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):1–15
Pflugmacher S, Schröder P Jr, Sandermann H (2000) Taxonomic distribution of plant glutathione S-transferases acting on xenobiotics. Phytochemistry 54(3):267
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):1–22
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):53–68
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101
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):125
Soonyoung A, Seonae K, Yun HK (2016) Glutathione S-transferase genes differently expressed by pathogen-infection in Vitis flexuosa. Plant Breed Biotechnol 4(5):61–70
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 271:511–521
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):3749
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):467
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):515
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):650
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):265
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):681–692
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 104:304–311
Acknowledgements
Thanks to Dr. Chen Jishan and Dr. Ma Jun from Heilongjiang Academy of Agricultural Sciences for their help in data analysis.
Funding
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).
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Ma, L., Zhang, Y., Meng, Q. et al. Molecular cloning, identification of GSTs family in sunflower and their regulatory roles in biotic and abiotic stress. World J Microbiol Biotechnol 34, 109 (2018). https://doi.org/10.1007/s11274-018-2481-0
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DOI: https://doi.org/10.1007/s11274-018-2481-0