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Trees

, Volume 32, Issue 3, pp 847–853 | Cite as

GSNOR deficiency enhances betulin production in Betula platyphylla

  • Guizhi FanEmail author
  • Tingting Nie
  • Yating Huang
  • Yaguang Zhan
Original Article

Abstract

Key message

This paper showed that GSNOR mediated betulin production from genetic and pharmacological levels.

Abstract

The aim of this study was to investigate the relationship between S-nitrosoglutathione reductase (GSNOR) and betulin production. Treatment of birch suspension cells with 20 μmol/L GSNOR inhibitor 3-(5-(4-(1H-imidazol-1-yl) phenyl)-1-(4-carbamoyl-2-methylphenyl)-1H-pyrrol-2-yl) propio- nic acid (N6022) markedly reduced gene expression of GSNOR, and increased at least two times in betulin content and gene expression of lupeol synthase (LUS), a key enzyme in betulin biosynthesis. GSNOR transgenic plants by RNAi silencing also lowered gene expression of GSNOR and increased betulin content and gene expression of LUS. Our study also showed that S-nitrosothiols (SNO) content increased in birch suspension cells treated with N6022 and GSNOR transgenic birch plants, about three times that in the non-transgenic birch. The above results verified that GSNOR deficiency mediated betulin production from genetic and pharmacological levels, and indicated that protein S-nitrosylation mediated plant secondary metabolite production.

Keywords

Betula platyphylla GSNOR SNO Betulin 

Notes

Acknowledgements

This work was supported by the Fundamental Research Funds for the Central Universities (2572017EA05), Heilongjiang Natural Science Foundation of China (C2016005), and Harbin Technological Innovation Special Fund research Projects (2014RFQXJ066).

Author contribution statement

Guizhi Fan and Yaguang Zhan conceived and designed the experiments. Tingting Nie and Yating Huang performed the experiments and collected the data. Yating Huang analyzed the data. Guizhi Fan wrote the paper.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

468_2018_1677_MOESM1_ESM.docx (170 kb)
Supplementary material 1 (DOCX 170 KB)

References

  1. Airaki M, Sánchez-Moreno L, Leterrier M, Barroso JB, Palma JM, Corpas FJ (2011) Detection and quantification of S-Nitrosoglutathione (GSNO) in Pepper (Capsicum annuum L.) Plant Organs by LC-ES/MS. Plant Cell Physiol 52(11):2006–2015CrossRefPubMedGoogle Scholar
  2. Alam P, Mohammad A, Ahmad MM, Khan MA, Nadeem M, Khan R, Akmal M, Ahlawat S, Abdin MZ (2014) Efficient method for Agrobacterium mediated transformation of Artemisia annua L. Recent Pat Biotechnol 8(1):102–107CrossRefPubMedGoogle Scholar
  3. Anand P, Hausladen A, Wang YJ, Zhang GF, Stomberski C, Brunengraber H, Hess DT, Stamler JS (2014) Identification of S-nitroso-CoA reductases that regulate protein S-nitrosylation. Proc Natl Acad Sci USA 111:18572–18577CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57(8):1785–1793CrossRefPubMedGoogle Scholar
  5. Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62(6):1803–1813CrossRefPubMedGoogle Scholar
  6. Fan GZ, Zhai QL, Zhan YG (2013) Gene expression of lupeol synthase and biosynthesis of nitric oxide in cell suspension cultures of Betula platyphylla in response to a phomopsis elicitor. Plant Mol Biol Rep 31:296–302CrossRefGoogle Scholar
  7. Fan GZ, Liu YT, Wang XD, Zhan YG (2014) Cross-talk of polyamines and nitric oxide in endophytic fungus-induced betulin production in Betula platyphylla plantlets. Trees Struct Funct 28:635–641CrossRefGoogle Scholar
  8. Fan GZ, Nie TT, Fan JS, Zhan YG (2017) Exogenous feeding of fructose and phenylalanine further improves Betulin Production in suspended Betula platyphylla Cells under Nitric Oxide Treatment. Molecules 22(1035):4–11Google Scholar
  9. Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fernández MR, Biosca JA, Parés X (2003) S-nitrosoglutathione reductase activity of human and yeast glutathione-dependent formaldehyde dehydrogenase and its nuclear and cytoplasmic localisation. Cell Mol Life Sci 60:1013–1018CrossRefPubMedGoogle Scholar
  11. Frungillo L, de Oliveira JFP, Saviani EE, Oliveira HC, Martínez MC, Salgado I (2013) Modulation of mitochondrial activity by S-nitrosoglutathione reductase in Arabidopsis thaliana transgenic cell lines. Biochimica et Biophysica Acta 1827:239–247CrossRefPubMedGoogle Scholar
  12. Guerra D, Ballard K, Truebridge I, Vierling E (2016) S-Nitrosation of conserved cysteines modulates activity and stability of S-nitrosoglutathione reductase (GSNOR). Biochem 55(17):2452–2464CrossRefGoogle Scholar
  13. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapink A, Bot NL, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421(6920):231–237CrossRefPubMedGoogle Scholar
  14. Kessler JH, Mullauer FB, de Roo GM, Medema JP (2007) Broad in vitro efficacy of plant-derived betulinic acid against cell lines derived from the most prevalent human cancer types. Cancer Lett 251:132–145CrossRefPubMedGoogle Scholar
  15. Kubienová L, Kopečný D, Tylichová M, Briozzo P, Skopalová J, Šebela M, Navrátil M, Tâche R, Luhová L, Barroso JB, Petřivalský M (2013) Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie 95:889–902CrossRefPubMedGoogle Scholar
  16. Kubienová L, Tichá T, Jahnová J, Luhová L, Mieslerová B, Petřivalský M (2014) Effect of abiotic stress stimuli on S nitrosoglutathione reductase in plants Planta 239:139–146CrossRefPubMedGoogle Scholar
  17. Kwon E, Feechan A, Yun BW, Hwang BH, Pallas JA, Kang JG, Loake GJ (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236(3):887–900CrossRefPubMedGoogle Scholar
  18. Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20:786–802CrossRefPubMedPubMedCentralGoogle Scholar
  19. Leterrier M, Chaki M, Airaki M, Valderrama R, Palma JM, Barroso JB, Corpas FJ (2011) Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal Behav 6(6):789–793CrossRefPubMedPubMedCentralGoogle Scholar
  20. Li X, Zhang L, Ahammed GJ, Li ZX, Wei JP, Shen C, Yan P, Zhang LP, Han WY (2017) Nitric oxide mediates brassinosteroid-induced flavonoid biosynthesis in Camellia sinensis L. J Plant Physiol 214:145–151CrossRefPubMedGoogle Scholar
  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time uantitative PCR and the \(2^{-\Delta \Delta C_{\text{T}}}\) method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  22. Malik SI, Hussain A, Yun BW, Spoel SH, Loake GJ (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181(5):540–544CrossRefPubMedGoogle Scholar
  23. Martínez MC, Achkor H, Persson B, Fernández MR, Shafqat J, Farré J, Jörnvall H, Parés X (1996) Arabidopsis formaldehyde dehydrogenase. Molecular properties of plant class III alcohol dehydrogenase provide further insights into the origins, structure and function of plant class p and liver class I alcohol dehydrogenases. Eur J Biochem 241:849–857CrossRefPubMedGoogle Scholar
  24. Rastogi S, Pandey MM, Rawat AKS (2015) Medicinal plants of the genus Betula—traditional uses and a phytochemical–pharmacological. J Ethnopharmacol 159:62–83CrossRefPubMedGoogle Scholar
  25. Rizzaa S, Filomeni G (2017) Chronicles of a reductase: biochemistry, genetics and physio-pathological role of GSNOR. Free Radic Bio Med 110:19–30CrossRefGoogle Scholar
  26. Rodríguez-Ruiz M, Mioto P, Palma JM, Corpas FJ (2017) S-nitrosoglutathione reductase (GSNOR) activity is down-regulated during pepper (Capsicum annuum L.) fruit ripening. Nitric Oxide 68:51–55CrossRefPubMedGoogle Scholar
  27. Salgado I, Martínez MC, Oliveira HC, Frungillo L (2013) Nitric oxide signaling and homeostasis in plants: a focus on nitrate reductase and S-nitrosoglutathione reductase in stress-related responses. Braz J Bot 36(2):89–98CrossRefGoogle Scholar
  28. Schulman IH, Hare JM (2012) Regulation of cardiovascular cellular processes by S-nitrosylation. Biochim Biophys Acta 1820(6):752–762CrossRefPubMedGoogle Scholar
  29. Shi YF, Wang DL, Wang C, Culler AH, Kreiser MA, Suresh J, Cohen JD, Pan JW, Baker B, Liu JZ (2015) Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol Plant 8(9):1350–1365CrossRefPubMedGoogle Scholar
  30. Suresh C, Zhao H, Gumbs A, Chetty CS, Bose HS (2012) New ionic derivatives of betulinic acid as highly potent anti-cancer agents. Bioorg Med Chem Lett 22:1734–1738CrossRefPubMedGoogle Scholar
  31. Tichá T, Cincalová L, Kopečný D, Sedlářová M, Kopečná M, Luhová L, Petřivalský M (2017) Characterization of S-nitrosoglutathione reductase from Brassica and Lactuca spp. and its modulation during plant development. Nitric Oxide 68:68–76CrossRefPubMedGoogle Scholar
  32. Wink DA, Kim S, Coffin D, Cook JC, Vodovotz Y, Chistodoulou D, Jourd’heuil D, Grisham MB (1999) Detection of S-nitrosothiols by fluorometric and colorimetric methods. Method Enzymol 301:201–211CrossRefGoogle Scholar
  33. Xu MJ, Dong J, Zhu MY (2005) Nitric oxide mediates the fungal elicitor-induced hypericin production of Hypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiol 139:991–998CrossRefPubMedPubMedCentralGoogle Scholar
  34. Xu MJ, Zhu Y, Dong JF, Jin HH, Sun L, Wang ZA, Lu ZH, Zhang M, Lu D (2012) Ozone induces flavonol production of Ginkgo biloba cells dependently on nitrate reductase-mediated nitric oxide signaling. Environ Exp Bot 75(75):114–119CrossRefGoogle Scholar
  35. Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101(1):25–33CrossRefPubMedGoogle Scholar
  36. Zeng FS, Sun FK, Li LL, Liu K, Zhan YG (2014) Genome-scale transcriptome analysis in response to nitric oxide in birch cells: implications of the triterpene biosynthetic pathway. PLoS ONE 9:116–157Google Scholar
  37. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23(4):283–333CrossRefPubMedGoogle Scholar
  38. Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol Bioch 68:118–126CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Life ScienceNortheast Forestry UniversityHarbinChina

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