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Nitric oxide mediates the fungal elicitor-induced puerarin biosynthesis in Pueraria thomsonii Benth. suspension cells through a salicylic acid (SA)-dependent and a jasmonic acid (JA)-dependent signal pathway

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Abstract

Nitric oxide (NO) has emerged as a key signaling molecule in plant secondary metabolite biosynthesis recently. In order to investigate the molecular basis of NO signaling in elicitor-induced secondary metabolite biosynthesis of plant cells, we determined the contents of NO, salicylic acid (SA), jasmonic acid (JA), and puerarin in Pueraria thomsonii Benth. suspension cells treated with the elicitors prepared from cell walls of Penicillium citrinum. The results showed that the fungal elicitor induced NO burst, SA accumulation and puerarin production of P. thomsonii Benth. cells. The elicitor-induced SA accumulation and puerarin production was suppressed by nitric oxide specific scavenger cPITO, indicating that NO was essential for elicitor-induced SA and puerarin biosynthesis in P. thomsonii Benth. cells. In transgenic NahG P. thomsonii Benth. cells, the fungal elicitor also induced puerarin biosynthesis, NO burst, and JA accumulation, though the SA biosynthesis was impaired. The elicitor-induced JA accumulation in transgenic cells was blocked by cPITO, which suggested that JA acted downstream of NO and its biosynthesis was controlled by NO. External application of NO via its donor sodium nitroprusside (SNP) enhanced puerarin biosynthesis in transgenic NahG P. thomsonii Benth. cells, and the NO-triggered puerarin biosynthesis was suppressed by JA inhibitors IBU and NDGA, which indicated that NO induced puerarin production through a JA-dependent signal pathway in the transgenic cells. Exogenous application of SA suppressed the elicitor-induced JA biosynthesis and reversed the inhibition of IBU and NDGA on elicitor-induced puerarin accumulation in transgenic cells, which indicated that SA inhibited JA biosynthesis in the cells and that SA might be used as a substitute for JA to mediate the elicitor-and NO-induced puerarin biosynthesis. It was, therefore, concluded that NO might mediate the elicitor-induced puerarin biosynthesis through SA-and JA-dependent signal pathways in wildtype P. thomsonii Benth. cells and transgenic NahG cells respectively.

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References

  1. Verpoorte R, Alfermann A W. Metabolic Engineering of Plant Secondary Metabolism. Dordrecht (The Netherlands): Kluwer Academic Publishers, 2000. 1–29

    Google Scholar 

  2. Roberts S C, Shuler M L. Large-scale plant cell culture. Curr Op Biotechnol, 1997, 8: 154–159

    Article  CAS  Google Scholar 

  3. Yu S W, Ou-Yang G C. The material basis of plant pathogenic resistance. In: Yu S W, Tang Z C, eds. Plant Physiology and Molecular Biology (in Chinese). Beijing: Science Press, 1999. 770–783

    Google Scholar 

  4. Ebel J, Scheel D. Elicitor recognition and signal transduction. In: Boller T, Meins F, eds, Genes Involved in Plant Defense. New York: Springer-Verlag, 1992. 183–205

    Google Scholar 

  5. Ciddi V, Srinivasan V, Shuler M L. Elicitation of Taxus sp. cell cultures for production of taxol. Biotechnol Lett, 1995, 17: 1343–1346

    Article  CAS  Google Scholar 

  6. Li C, Yuan Y J, Ma Z H, Hu Z D. Changes of physiological state of suspension cultures of Taxus chinensis var. mairei induced by oligosarchride. J Chem Indus Engineer (in Chinese), 2002, 53(11): 1133–1138

    CAS  Google Scholar 

  7. Dietrich A, Mayer J E, Hahlbrock K. Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. J Biol Chem, 1990, 265: 6360–6368

    PubMed  CAS  Google Scholar 

  8. Nürnberger T, Colling C, Hahlbrock K, Jabs T, Renelt A, Sacks W R, Scheel D. Perception and transduction of an elicitor signal in cultured parsley cells. Biochem Soc Symp, 1994, 60: 173–182

    PubMed  Google Scholar 

  9. Baker C J, Orlandi E W. Active oxygen in plant pathogenesis. Annu Rev Phytopathol, 1995, 33: 299–321

    Article  CAS  Google Scholar 

  10. Neill S J, Desikan R, Hancock J T. Nitric oxide signaling in plants. New Phytologist, 2003, 159: 11–22

    Article  CAS  Google Scholar 

  11. Morot-Gaudry-Talarmain Y, Rockel P, Moureaux T, Quillere I, Leydecker M T, Kaiser W M, Morot-Gaudry J F. Nitrite accumulation and nitric oxide emission in relation to cellular signaling in nitrite reductase antisense plants. Planta, 2002, 215: 708–715

    Article  PubMed  CAS  Google Scholar 

  12. Beligni M V, Lamattina L, Nitric oxide stimulates seed germination and deetiolation, and inhibits hypocotyls elongation, three light-inducible responses in plants. Planta, 2000, 210: 215–222

    Article  PubMed  CAS  Google Scholar 

  13. Delledonne M, Zeier J, Marocco A, Lamb C. Signal interaction between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA, 2001, 98: 13454–13459

    Article  PubMed  CAS  Google Scholar 

  14. Modolo L V, Cunha F Q, Braga M R, Salgado I. Nitric oxide synthase-mediated phytoalexin accumulation in soybean cotyledons in response to the Diaporthe phaseolorum f. sp. meridionalis elicitor. Plant Physiol, 2002, 130: 1288–1297

    Article  PubMed  CAS  Google Scholar 

  15. Durner J, Wendehenne D, Klessig D F. Defense gene induction in tobacco by nitric oxide, cyclic CMP and cyclic ADP-ribose. Proc Natl Acad Sci USA, 1998, 95: 10328–10333

    Article  PubMed  CAS  Google Scholar 

  16. Xu M J, Dong J, Zhu M. Effect of nitric oxide on catharanthine production and growth of Catharanthus roseus suspension cells. Biotechol Bioeng, 2005, 89(3): 367–371

    Article  CAS  Google Scholar 

  17. Xu M J, Dong J F, Zhu M Y. Involvement of NO in elicitor-induced PAL activation and Taxol synthesis stimulation of Taxus chinensis suspension cells. Chin Sci Bull, 2004, 49(10): 1038–1043

    Article  CAS  Google Scholar 

  18. Xu M J, Dong J. Elicitor-induced nitric oxide burst is essential for triggering catharanthine synthesis in Catharanthus roseus suspension cells. Appl Microbiol Biotechnol, 2005, 67(1): 40–44

    Article  PubMed  CAS  Google Scholar 

  19. Kechum R E B. The kinetics of Taxol accumulation in cell suspension cultures of Taxus following elicitation with methyl jasmonate. Biotechol Bioeng, 1999, 62(1): 97–105

    Article  Google Scholar 

  20. Creelman R A, Mullet J E. Biosynthesis and action of jasmonates in plants. Annu Rev Plant Mol Biol, 1997, 48: 355–381

    Article  CAS  Google Scholar 

  21. Ellard-Ivey M, Douglas C J. Role of jasmonates in the elicitor-and wound-inducible expression of defense genes in parsley and transgenic tobacco. Plant Physiol, 1996, 112: 183–192

    PubMed  CAS  Google Scholar 

  22. Menke F L H, Parchmann S, Mueller M J, Kijne J W, Memelink J. Involvement of the Octadecanoid Pathway and Protein Phosphorylation in Fungal Elicitor-Induced Expression of Terpenoid Indole Alkaloid Biosynthetic Genes in Catharanthus roseus. Plant Physiol, 1999, 119: 1289–1296

    Article  PubMed  CAS  Google Scholar 

  23. Nojiri H, Sugimori M, Yamane H, Nishimura Y, Yamada A, Shibuya N, Kodama O, Murofushi N, Omori T. Involvement of jasmonic acid in elicitor-induced phytoalexin production in suspension-cultured rice cells. Plant Physiol, 1996, 110: 387–392

    PubMed  CAS  Google Scholar 

  24. Mueller M J, Brodschelm W, Spannagl E, Zenk M H. Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc Natl Acad Sci USA, 1993, 90: 7490–7494

    Article  PubMed  CAS  Google Scholar 

  25. Shah J. The salicylic acid loop in plant defense. Curr Opin Plant Biol, 2003, 6: 365–371

    Article  PubMed  CAS  Google Scholar 

  26. Thomma B P, Penninckx I A, Broekaert W F, Cammue B P. The complexity of disease signaling in Arabidopsis. Curr Opin Immunol, 2001, 13: 63–68

    Article  PubMed  CAS  Google Scholar 

  27. Gamborg O L, Miller R A, Ojima K. Nutrient requirements of suspension culture of soybean root cultures. Exp Cell Res, 1968, 50: 151–158

    Article  PubMed  CAS  Google Scholar 

  28. Zhang C H, Mei X G, Liu L, Zhang J. Enhanced paclitaxel production induced by the combination of elicitors in cell suspension cultures of Taxus chinensis. Biotechnol Lett, 2000, 22: 1561–1564

    Article  CAS  Google Scholar 

  29. Hu X Y, Neill S J, Cai W M, Tang Z C. NO-mediated hypersensitive responses of rice suspension cultures induced by incompatible elicitor. Chin Sci Bull, 2003, 48(4): 358–363

    Article  CAS  Google Scholar 

  30. Delledonne M, Xia Y, Dixon R A. Lamb C. Nitric oxide functions as a secondary signal in plant disease resistance. Nature, 1998, 394: 585–588

    Article  PubMed  CAS  Google Scholar 

  31. Alami I, Jouy N, Clervet A. The lipoxygenase pathway is involved in elicitor-induced phytoalexin accumulation in plane tree (Platanus acerifolia) cell-suspension cultures. J Phytopathol, 1999, 147: 515–519

    Article  CAS  Google Scholar 

  32. Meuwly P, Metraux J P. Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal Biochem, 1993, 214: 500–505

    Article  PubMed  CAS  Google Scholar 

  33. Fournier J, Pouenat M L, Rickaner M. Purification and characterization of elicitor-induced lipoxygenase in tobacco cells. Plant J, 1993, 3: 63–70

    CAS  Google Scholar 

  34. Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle fo protein-dye binding. Anal Biochem, 1976, 72: 248–254

    Article  PubMed  CAS  Google Scholar 

  35. He J T, Shi Z H, Zhao M P, Chang W B. Determination of Puerarin and Daidzein by reversed phase HPLC. Chin J Analyt Chem, 2004, 32(4): 519–521

    CAS  Google Scholar 

  36. Camera L S, Gouzerh G, Dhondt S, Hoffmann L, Fritig B, Legrand M, Heitz T. Metabolic reprogramming in plants innate immunity: The contributions of phenylpropaniod and oxylipin pathways. Immunol Rev, 2004, 198: 267–284

    Article  PubMed  Google Scholar 

  37. Tabata H. Paclitaxel production by plant-cell-culture technology. Adv Biochem Eng Biotechnol, 2004, 87: 1–23

    PubMed  CAS  Google Scholar 

  38. Sanchez-Sampedro M A, Fernandez-Tarrago J, Corchete P. Yeast extract and methyl jasmonate-induced silymarin production in cell cultures of Silybum marianum (L.) Gaertn, J Biotechnol, 2005, 119(1): 60–69

    Article  PubMed  CAS  Google Scholar 

  39. Suzuki H, Reddy M S, Naoumkina M, Aziz N, May G D, Huhman D V, Sumner L W, Blount J W, Mendes P, Dixon R A. Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta, 2005, 220(5): 696–707

    Article  PubMed  CAS  Google Scholar 

  40. Mei X G. Production of Taxol by Taxus chinensis Cell Cultures (in Chinese). Wuhan: Press of the Scientific University of Central China, 2003. 50–89

    Google Scholar 

  41. Yukimune Y, Tabata H, Higashi Y, Hara Y. Methyl jasmonate-induced over production of paclitaxel and baccation III in taxus cell suspension cultures. Nature Biotechnology, 1996, 14: 1129–1132

    Article  PubMed  CAS  Google Scholar 

  42. Huang X, Stettmaier K, Michel C, Hutzler P, Mueller M J M, Durner J. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta, 2004, 218(6): 938–946

    Article  PubMed  CAS  Google Scholar 

  43. Kunkel B N, Brooks D M. Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol, 2002, 5: 325–331

    Article  PubMed  CAS  Google Scholar 

  44. Creelman R A, Mullet J E. Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol, 1997, 48: 355–381

    Article  PubMed  CAS  Google Scholar 

  45. Seo S, Sano H, Ohashi Y. Jasmonic acid in wound signal transduction pathways. Physiol Plant, 1997, 101: 740–745

    Article  CAS  Google Scholar 

  46. Spoel S H. NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell, 2003, 15: 760–770

    Article  PubMed  CAS  Google Scholar 

  47. Gupta V, Willits M G, Glazebrook J. Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of dsefense responses: Evidence for inhibition of jasmonic acid signaling by SA. Mol Plant-Microbe Interact, 2000, 13: 503–511

    PubMed  CAS  Google Scholar 

  48. Niki T, Mitsuhara I, Seo S, Hidaka H. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol, 1998, 39: 500–507

    CAS  Google Scholar 

  49. Ribeiro E A Jr., Cunha F Q, Tamashiro W M, Martins I S. Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells. FEBS Lett, 1999, 445(2–3): 283–286

    Article  PubMed  CAS  Google Scholar 

  50. Foissner I, Wendehenne D, Langebartels C, Durner J. In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J, 2000, 23(6): 817–824

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biotechnology, Zhejiang Gongshang University, Hangzhou, 310035, China

    Xu Maojun & Dong Jufang

  2. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, 310012, China

    Zhu Muyuan

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  1. Xu Maojun
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  2. Dong Jufang
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Correspondence to Xu Maojun.

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Xu, M., Dong, J. & Zhu, M. Nitric oxide mediates the fungal elicitor-induced puerarin biosynthesis in Pueraria thomsonii Benth. suspension cells through a salicylic acid (SA)-dependent and a jasmonic acid (JA)-dependent signal pathway. SCI CHINA SER C 49, 379–389 (2006). https://doi.org/10.1007/s11427-006-2010-5

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  • DOI: https://doi.org/10.1007/s11427-006-2010-5

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