Year 2020, Volume 79 , Issue 2, Pages 89 - 97 2020-12-25

Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity

Mustafa YILDIZ [1] , Melike CELIK [2] , Hakan TERZI [3]


Objective: The salinization of agricultural soils poses a serious challenge across the world. Although recent studies have shown that exogenous sodium nitroprusside (SNP) application can alleviate the harmful effects of salinity, the roles of SNP in the regulation of proteomic changes remain poorly understood. Materials and Methods: To unravel the protective roles of exogenous SNP in alleviating salt-induced damage in barley (Hordeum vulgare L.), proteomic analysis was carried out on the leaves of seedlings exposed to 100 mM NaCl stress following 200 M SNP pre-treatment. Results: Our results indicated that SNP pre-treatment restored the seedling growth reduced by salinity stress. Comparing 2-DE gels from the treatments showed that 24 proteins were differentially accumulated under SNP and/or NaCl stress treatments. Among them, 15 proteins were identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Gene ontology analysis demonstrated that several pathways were regulated by SNP and/or NaCl treatments, including photosynthesis, protein metabolism, stress defense, and energy metabolism. Exogenous SNP increased the expression levels of 20 kDa chaperonin, proteasome subunit beta type-2, 2-Cys peroxiredoxin BAS1, ferredoxin-NADP reductase, thiazole biosynthetic enzyme 1-1, S-adenosylmethionine synthetase 3, and elongation factor Tu proteins in the leaves of barley seedlings under NaCl stress. Conclusion: Our results indicate that SNP pre-treatment may induce salinity tolerance growth inhibition through regulation of photosynthesis, activation of stress defence, degradation of damaged proteins, and the promoting of the synthesis of polyamines, proline, and GABA
Barley, Nitric oxide, Salinity stress, Sodium nitroprusside, Proteomics
  • 1. Munns R, Tester M. Mechanisms of salinity tolerance. Ann Rev Plant Biol 2008; 59: 651–81.
  • 2. Setia R, Gottschalk P, Smith P, Marschner P, Baldock J, Setia D et al., Soil salinity decreases global soil organic carbon stocks. Sci Total Environ 2013; 465: 267–72.
  • 3. Soundararajan P, Manivannan A, Ko CH, Muneer S, Jeong BR. Leaf physiological and proteomic analysis to elucidate silicon induced adaptive response under salt stress in rosa hybrida ‘rock fire.’ Int J Mol Sci 2017; 18(8).
  • 4. Ahmad P, Abass AM, Nasser AM, Wijaya L, Alam P, Ashraf M. Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. J Plant Interact 2018; 13(1): 64–72.
  • 5. Hasanuzzaman M, Oku H, Nahar K, Bhuyan MHMB, Al Mahmud J, Baluska F et al., Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions. Plant Biotechnol Rep 2018; 12(2): 77–92.
  • 6. Fancy NN, Bahlmann AK, Loake GJ. Nitric oxide function in plant abiotic stress. Plant Cell Environ 2017; 40(4): 462–72.
  • 7. Ali Q, Daud MK, Haider MZ, Ali S, Rizwan M, Aslam N et al., Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters. Plant Physiol Biochem 2017; 119: 50–8.
  • 8. Yadu S, Dewangan TL, Chandrakar V, Keshavkant S. Imperative roles of salicylic acid and nitric oxide in improving salinity tolerance in Pisum sativum L. Physiol Mol Biol Plants 2017; 23(1): 43–58.
  • 9. Wu XX, Zhu XH, Chen JL, Yang SJ, Ding HD, Zha DS. Nitric oxide alleviates adverse salt-induced effects by improving the photosynthetic performance and increasing the anti-oxidant capacity of eggplant (Solanum melongena L.), J Hortic Sci Biotech 2015; 88(3): 352–60.
  • 10. Fatma M, Khan NA. Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot 2014; 4: 106–16.
  • 11. Bai X, Yang L, Yang Y, Ahmad P, Yang Y, Hu X. Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J Proteome Res 2011; 10: 4349–64.
  • 12. Shen Z, Chen J, Ghoto K, Hu W, Gao G, Luo M et al., Proteomic analysis on mangrove plant Avicennia marina leaves reveals nitric oxide enhances the salt tolerance by up-regulating photosynthetic and energy metabolic protein expression, Tree Physiol 2018; 38 (11): 1605–22.
  • 13. Ahsan N, Lee DG, Alam I, Kim PJ, Lee JJ, Ahn YO et al., Comparative proteomic study of arsenic-induced differentially expressed proteins in rice roots reveals glutathione plays a central role during As stress. Proteomics 2008; 8: 3561–76.
  • 14. Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 1976; 72: 248–54.
  • 15. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B et al., Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004; 25: 1327–33.
  • 16. Sinha P, Poland J, Schnölzer M, Rabilloud T. A new silver staining apparatus and procedure for matrix-assisted laser desorption/ionization-time of flight analysis of proteins after two-dimensional electrophoresis. Proteomics 2001; 1: 835–40.
  • 17. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P et al., The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011; 39: 561–8.
  • 18. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in biological networks. Bioinformatics 2005; 21: 3448–9.
  • 19. Terrón-Camero LC, Peláez-Vico MÁ, Del-Val C, Sandalio LM, Romero-Puertas MC. Role of nitric oxide in plant responses to heavy metal stress: exogenous application versus endogenous production. J Exp Bot 2019; 70(17): 4477–88.
  • 20. Tripathi DK, Singh S, Singh S, Srivastava PK, Singh VP, Singh S et al., Nitric oxide alleviates silver nanoparticles (AgNps)-induced phytotoxicity in Pisum sativum seedlings. Plant Physiol Biochem 2017; 110: 167–77.
  • 21. Leshem YY, Haramaty E. Plant aging: the emission of NO and ethylene and effect of NO-releasing compounds on growth of pea (Pisum sativum) foliage. J Plant Physiol 1996; 148: 258–63.
  • 22. Dong YJ, Jinc SS, Liu S, Xu LL, Kong J. Effects of exogenous nitric oxide on growth of cotton seedlings under NaCl stress. J Soil Sci Plant Nutr 2014; 14: 1–13.
  • 23. Mostofa MG, Fujita M, Tran LSP. Nitric oxide mediates hydrogen peroxide- and salicylic acid-induced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul 2015; 77: 265–77.
  • 24. Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 2009; 103(4): 551–60.
  • 25. de Abreu CE, Araujo Gdos S, Monteiro-Moreira AC, Costa JH, Leite Hde B, Moreno FB et al., Proteomic analysis of salt stress and recovery in leaves of Vigna unguiculata cultivars differing in salt tolerance. Plant Cell Rep 2014; 33(8): 1289–306.
  • 26. Fukuyama K. Structure and function of plant type ferredoxins. Photosynth Res 2004; 81:289–301.
  • 27. Musumeci MA, Ceccarelli A, Catalano-Dupuy DL. The plant–type ferredoxin-NADP+ reductases. Najafpour M, editor. Advances in Photosynthesis-Fundamental Aspects; InTech: Rijeka, Croatia; 2012; pp. 539–62.
  • 28. Rodriguez RE, Lodeyro A, Poli HO, Zurbriggen M, Peisker M, Palatnik JF et al., Transgenic tobacco plants overexpressing chloroplastic ferredoxin-NADP(H) reductase display normal rates of photosynthesis and increased tolerance to oxidative stress. Plant Physiol 2007; 143(2): 639–49.
  • 29. Wang M, Xu Q, Yuan M. The unfolded protein response induced by salt stress in Arabidopsis. Method Enzymol 2011; 489: 319–28.
  • 30. Peng HT, Li YX, Zhang CW, Li Y, Hou XL. Chloroplast elongation factor BcEF-Tu responds to turnip mosaic virus infection and heat stress in non-heading Chinese cabbage. Biol Plant 2014; 58(3): 561–6.
  • 31. Roy S, Mishra M, Dhankher OP, Singla-Pareek SL, Pareek A. Molecular Chaperones: Key players of abiotic stress response in plants. Rajpal V, Sehgal D, Kumar A, Raina S, editors. Genetic Enhancement of Crops for Tolerance to Abiotic Stress: Mechanisms and Approaches, Vol. I. Sustainable Development and Biodiversity, vol 20. Springer.2019.
  • 32. Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin Q et al., Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell 2012; 24: 233–44.
  • 33. Hossain MS, Dietz KJ. Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Front Plant Sci 2016; 7: 548.
  • 34. Kim SY, Jang HH, Lee JR, Sung NR, Bin Lee H, Lee DH et al., Oligomerization and chaperone activity of a plant 2-Cys peroxiredoxin in response to oxidative stress. Plant Sci 2009; 177(3): 227–32.
  • 35. Machado CR, de Oliveira RL, Boiteux S, Praekelt UM, Meacock PA, Menck CF. Thi1, a thiamine biosynthetic gene in Arabidopsis thaliana, complements bacterial defects in DNA repair. Plant Mol Biol 1996; 31(3): 585–93.
  • 36. Ribeiro DT, Farias LP, de Almeida JD, Kashiwabara PM, Ribeiro AF, Silva-Filho MC et al., Functional characterization of the thi1 promoter region from Arabidopsis thaliana. J Exp Bot 2005; 56(417): 1797–804.
  • 37. Rapala-Kozik M, Wolak N, Kujda M, Banas AK. The upregulation of thiamine (vitamin B1) biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is mediated by abscisic acid at the early stages of this stress response. BMC Plant Biol 2012; 12: 2.
  • 38. Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y et al., Mechanisms of plant salt response: insights from proteomics. J Proteome Res 2012; 11: 49–67.
  • 39. Yin H, Li S, Zhao X, Bai X, Du Y. Isolation and characterization of an oilseed rape SKP1 gene BnSKP1 involved on defence in Brassica napus. J Biotechnol 2008; 136: S227.
  • 40. Fan W, Zhang ZL, Zhang YL. Cloning and molecular characterization of fructose-1,6-bisphosphate aldolase gene regulated by high-salinity and drought in Sesuvium portulacastrum. Plant Cell Rep 2009; 28: 975–84.
  • 41. Gong B, Li X, VandenLangenberg KM, Wen D, Sun S, Wei M et al., Overexpression of S-adenosyl-L-methionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism. Plant Biotechnol J 2014; 12: 694–708.
  • 42. Qi YC, Wang FF, Hui Z, Liu WQ. Overexpression of Suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco. Acta Physiol Plant 2010; 32: 263–9.
  • 43. Witzel K, Weidner A, Surabhi GK, Börner A, Mock H. Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot 2009; 60:3545–57.
  • 44. Gut H, Dominici P, Pilati S, Astegno A, Petoukhov MV, Svergun DI et al., A common structural basis for pH- and calmodulin-mediated regulation in plant glutamate decarboxylase. J Mol Biol 2009; 392: 334–51.
  • 45. Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A et al., The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 2010; 10: 20.
  • 46. Li Z, Cheng B, Zeng W, Zhang X, Peng Y. Proteomic and metabolomic profilings reveal crucial functions of γ-aminobutyric acid in regulating ionic, water, and metabolic homeostasis in creeping bentgrass under salt stress. J Proteome Res 2020; 19: 769–80.
  • 47. Zhang Y, Wei M, Liu A, Zhou R, Li D, Dossa K et al., Comparative proteomic analysis of two sesame genotypes with contrasting salinity tolerance in response to salt stress. J Proteomics 2019; 201: 73–83.
Primary Language en
Subjects Science
Journal Section Research Articles
Authors

Orcid: 0000-0002-6819-9891
Author: Mustafa YILDIZ (Primary Author)
Institution: AFYON KOCATEPE UNIVERSITY
Country: Turkey


Author: Melike CELIK
Institution: AFYON KOCATEPE UNIVERSITY
Country: Turkey


Author: Hakan TERZI
Institution: AFYON KOCATEPE UNIVERSITY
Country: Turkey


Supporting Institution The support of Afyon Kocatepe University Research Fund (Project No. 18.FEN.BİL.01) to this research is thankfully acknowledged.
Project Number 18.FEN.BİL.01
Thanks The authors gratefully acknowledge the Medicinal Genetics Laboratory of Afyonkarahisar Health Sciences University and the DEKART Proteomics Laboratory of Kocaeli University for their technical help. The authors also wish to thank Afyon Kocatepe University’s Foreign Language Support Unit for language editing.
Dates

Application Date : June 18, 2020
Acceptance Date : September 26, 2020
Publication Date : December 25, 2020

Bibtex @research article { iufsjb817025, journal = {European Journal of Biology}, issn = {2602-2575}, eissn = {2618-6144}, address = {}, publisher = {Istanbul University}, year = {2020}, volume = {79}, pages = {89 - 97}, doi = {}, title = {Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity}, key = {cite}, author = {Yıldız, Mustafa and Celık, Melike and Terzı, Hakan} }
APA Yıldız, M , Celık, M , Terzı, H . (2020). Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity . European Journal of Biology , 79 (2) , 89-97 . Retrieved from https://dergipark.org.tr/en/pub/iufsjb/issue/55111/817025
MLA Yıldız, M , Celık, M , Terzı, H . "Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity" . European Journal of Biology 79 (2020 ): 89-97 <https://dergipark.org.tr/en/pub/iufsjb/issue/55111/817025>
Chicago Yıldız, M , Celık, M , Terzı, H . "Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity". European Journal of Biology 79 (2020 ): 89-97
RIS TY - JOUR T1 - Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity AU - Mustafa Yıldız , Melike Celık , Hakan Terzı Y1 - 2020 PY - 2020 N1 - DO - T2 - European Journal of Biology JF - Journal JO - JOR SP - 89 EP - 97 VL - 79 IS - 2 SN - 2602-2575-2618-6144 M3 - UR - Y2 - 2020 ER -
EndNote %0 European Journal of Biology Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity %A Mustafa Yıldız , Melike Celık , Hakan Terzı %T Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity %D 2020 %J European Journal of Biology %P 2602-2575-2618-6144 %V 79 %N 2 %R %U
ISNAD Yıldız, Mustafa , Celık, Melike , Terzı, Hakan . "Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity". European Journal of Biology 79 / 2 (December 2020): 89-97 .
AMA Yıldız M , Celık M , Terzı H . Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity. Eur J Biol. 2020; 79(2): 89-97.
Vancouver Yıldız M , Celık M , Terzı H . Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity. European Journal of Biology. 2020; 79(2): 89-97.
IEEE M. Yıldız , M. Celık and H. Terzı , "Proteomic Analysis of the Protective Effect of Sodium Nitroprusside on Leaves of Barley Stressed by Salinity", European Journal of Biology, vol. 79, no. 2, pp. 89-97, Dec. 2020