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Volume 155, Issue 10

Nitric oxide mediates the fungal-elicitor-enhanced biosynthesis of antioxidant polyphenols in submerged cultures of Free

Abstract

A fungal elicitor prepared from the cell debris of the plant-pathogenic ascomycete induces multiple responses by cells, including an increase in generation of nitric oxide (NO), activity of phenylalanine ammonia lyase (PAL) and accumulation of total mycelial phenolic compounds (TMP), but does not trigger production of oxylipins or jasmonic acid (JA). The role of NO in TMP production was investigated via the effects of the NO-specific scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPITO) and the nitric oxide synthase (NOS) inhibitor aminoguanidine (AG). TMP profiles were assayed using H NMR spectroscopy combining multivariate pattern recognition strategies. Pretreatment of mycelia with cPITO or AG suppressed not only elicitor-enhanced NO generation and PAL activity, but also the elicitor-induced increase in TMP production. This TMP reduction by either a NO scavenger or a NOS inhibitor was reversed by exogenous addition of either a NO donor, sodium nitroprusside, or JA separately. NMR-based metabonomic analysis of TMP profiles showed that the induced TMP were hispidin analogues including inoscavins, phelligridins, davallialactone and methyldavallialactone, which possess high antioxidant activities. Thus, NO mediates an elicitor-induced increase in production of antioxidant polyphenols in via a signalling pathway independent of oxylipins or JA, a mechanism which differs from those in some higher plants.

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Keyword(s): AG, aminoguanidine , cPITO, 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide , DPPH, 1,1-diphenyl-2-picrylhydrazyl , JA, jasmonic acid , NOS, nitric oxide synthase , PAL, phenylalanine ammonia lyase , PC, principal component , PCA, principal component analysis , RO, reverse osmosis , SNP, sodium nitroprusside , TMP, total mycelial phenolic compounds and TMS, tetramethylsilane
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2009-10-01
2024-04-24
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References

  1. Assaf S., Hadar Y., Dosoretz C. G. 1995; Biosynthesis of 13-hydroperoxylinoleate, 10-oxo-8-decenoic acid, and 1-octen-3-ol from linoleic acid by a mycelial-pellet homogenate of Pleurotus pulmonarius . J Agric Food Chem 43:2173–2178
     [Google Scholar]
  2. Babitskaia V. G., Shcherba V. V., Ikonnikova N. V. 2000; Melanin complex of the fungus Inonotus obliquus . Prikl Biokhim Mikrobiol 36:439–444
     [Google Scholar]
  3. Baker C. J., Orlandi E. W. 1995; Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33:299–321
     [Google Scholar]
  4. Beckwith-Hall B. M., Holmes E., Lindon J. C., Gounarides J., Vickers A., Shapiro M., Nicholson J. K. 2002; NMR-based metabonomic studies on the biochemical effects of commonly used drug carrier vehicles in the rat. Chem Res Toxicol 15:1136–1141
     [Google Scholar]
  5. Bolwell P. P., Page A., Pislewska M., Wojtaszek P. 2001; Pathogenic infection and the oxidative defenses in plant apoplast. Protoplasma 217:20–32
     [Google Scholar]
  6. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
     [Google Scholar]
  7. Combet E., Henderson J., Eastwood D. C., Burton B. S. 2006; Eight-carbon volatiles in mushrooms and fungi: properties, analysis and biosynthesis. Mycoscience 47:317–326
     [Google Scholar]
  8. Durner J., Klessig D. F. 1999; Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374
     [Google Scholar]
  9. Foissner I., Wendehenne D., Longteraals P., Durner J. 2000; In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23:817–824
     [Google Scholar]
  10. Gao X. X., Ge H. M., Zheng W. F., Tan R. X. 2008; NMR-based metabonomics for detection of Helicobater pylori infection in gerbils: which is more descriptive. Helicobacter 13:103–111
     [Google Scholar]
  11. Ham S. S., Kim S. H., Moon S. Y., Chung M. J., Cui C. B., Han E. K., Chung C. K., Choe M. 2009; Antimutagenic effects of subfractions of Chago mushroom ( Inonotus obliquus) extract. Mutat Res 672:55–59
     [Google Scholar]
  12. Hoshino T., Tronsmo A. M., Matsumoto N., Araki T., Georges F., Goda T., Ohgiya S., Ishizaki K. 1998; Freezing resistance among isolates of a psychrophilic fungus, Typhula ishikariensis, from Norway. Proc NIPR Symp Polar Biol 11:112–118
     [Google Scholar]
  13. Jung J. Y., Lee I. K., Seok S. J., Lee H. J., Kim Y. H., Yun B. S. 2008; Antioxidant polyphenols from the mycelial culture of the medicinal fungi Inonotus xeranticus and Phellinus linteus . J Appl Microbiol 104:1824–1832
     [Google Scholar]
  14. Kim J.-P., Yun B.-S., Shim Y. K., Yoo I.-D. 1999; Inoscavin A, a new free radical scavenger from the mushroom Inonotus xeranticus . Tetrahedron Lett 40:6643–6644
     [Google Scholar]
  15. Kojima K., Ohno T., Inoue M., Mizukami H., Nagatsu A. 2008; Phellifuropyranone A: a new furopyranone compound isolated from fruit bodies of wild Phellinus linteus . Chem Pharm Bull (Tokyo 56:173–175
     [Google Scholar]
  16. Lee I. K., Yun B. S. 2006; Hispidin analogs from the mushroom Inonotus xeranticus and their free radical scavenging activity. Bioorg Med Chem Lett 16:2376–2379
     [Google Scholar]
  17. Lee I. K., Yun B. S. 2007; Highly oxygenated and unsaturated metabolites providing a diversity of hispidin class antioxidants in the medicinal mushrooms Inonotus and Phellinus . Bioorg Med Chem 15:3309–3314
     [Google Scholar]
  18. Lee I. K., Seok S. J., Kim W. K., Yun B. S. 2006; Hispidin derivatives from the mushroom Inonotus xeranticus and their antioxidant activity. J Nat Prod 69:299–301
     [Google Scholar]
  19. Lee I. K., Kim Y. S., Jang Y. W., Jung J. Y., Yun B. S. 2007; New antioxidant polyphenols from the medicinal mushroom Inonotus obliquus . Bioorg Med Chem Lett 17:6678–6681
     [Google Scholar]
  20. Li L., Wang J. N., Ren J., Xiang J. F., Tang Y. L., Liu J. X., Han D. 2007; Metabonomics analysis of the urine of rats with Qi deficiency and blood stasis syndrome based on NMR techniques. Chin Sci Bull 52:3068–3073
     [Google Scholar]
  21. Mo S., Wang S., Zhou G., Yang Y., Li Y., Chen X., Shi J. 2004; Phelligridins C-F: cytotoxic pyrano[4,3-c][2]benzopyran-1,6-dione and furo[3,2-c]pyran-4-one derivatives from the fungus Phellinus igniarius . J Nat Prod 67:823–828
     [Google Scholar]
  22. Modolo L. V., Cunha F. Q., Braga M. R., Salgado I. 2002; Nitric oxide synthase-mediated phytoalexin accumulation in soybean cotyledons in response to the Diaporthe phaseolorum f.sp. meridionalis elicitor. Plant Physiol 130:1288–1297
     [Google Scholar]
  23. Mori T., Sakurai M., Sakuta M. 2001; Effects of conditioned medium on activities of PAL, CHS, DAHP synthase (DS-Co and DS-Mn) and anthocyanin production in suspension cultures of Fragaria ananassa . Plant Sci 160:355–360
     [Google Scholar]
  24. Neill S. J., Desikan R., Clarke A., Hurst R. D., Hancock J. T. 2002; Hydrogen peroxide and nitric oxide as signal molecules in plants. J Exp Bot 53:1237–1247
     [Google Scholar]
  25. Nicholson J. K., Connelly J., Holmes E. 1999; “Metabonomics”: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29:1181–1189
     [Google Scholar]
  26. Noverr M. C., Erb-Downward J. R., Huffnage G. B. 2003; Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16:517–533
     [Google Scholar]
  27. Roberts S. C., Shuler M. L. 1997; Large-scale plant cell culture. Curr Opin Biotechnol 8:154–159
     [Google Scholar]
  28. Romero-Puertas M. C., Delledonne M. 2003; Nitric oxide signaling in plant-pathogen interactions. IUBMB Life 55:579–583
     [Google Scholar]
  29. Shyu Y.-S., Hwang L. S. 2002; Antioxidant activity of the crude extract of lignan glycosides from unroasted Burma black sesame meal. Food Res Int 35:357–365
     [Google Scholar]
  30. Singleton V. L., Rossi J. A. Jr 1965; Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158
     [Google Scholar]
  31. Song F. M., Goodman R. M. 2001; Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol Plant Microbe Interact 14:1458–1462
     [Google Scholar]
  32. Tsitsigiannis D. I., Keller N. P. 2007; Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–118
     [Google Scholar]
  33. Wang Y., Shang X. Y., Wang S. J., Mo S. Y., Li S., Yang Y. C., Ye F., Shi J. G., He L. 2007; Structures, biogenesis, and biological activities of pyrano[4,3-c]isochromen-4-one derivatives from the fungus Phellinus igniarius . J Nat Prod 70:296–299
     [Google Scholar]
  34. Xu M.-J., Dong J.-F., Zhu M.-Y. 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 139:991–998
     [Google Scholar]
  35. Zhao J., Davis L. C., Verpoorte R. 2005; Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333
     [Google Scholar]
  36. Zhao Y. X., Miao K. J., Sun W. G., Zhang M. M., Wei Z. W., Zheng W. F. 2009; Effects of jasmonic acid and hydrogen peroxide on production of phenolic compounds in a melanin-deficient mutant of Phaeoporus obliquus . Mycosystema 28:129–137
     [Google Scholar]
  37. Zheng W., Zhao Y., Miao K., Zhang M., Wei Z. 2008a; A new method for culturing Inonotus obliquus by liquid fermentation. State Intellectual Property Office of China CN200810227890 4:1–14
     [Google Scholar]
  38. Zheng W. F., Zhao Y. X., Zhang M. X., Yin Z. J., Chen C. F., Wei Z. W. 2008b; Phenolic compounds from Inonotus obliquus and their immune stimulating effects. Mycosystema 27:39–47
     [Google Scholar]
  39. Zheng W., Zhang M., Zhao Y., Wang Y., Miao K., Wei Z. 2009a; Accumulation of antioxidant phenolic constituents in submerged cultures of Inonotus obliquus . Bioresour Technol 100:1327–1335
     [Google Scholar]
  40. Zheng W., Zhao Y., Zhang M., Wei Z., Miao K., Sun W. 2009b; Oxidative stress response of Inonotus obliquus induced by hydrogen peroxide. Med Mycol, Jan 31: [Epub ahead of print]
    [Google Scholar]
  41. Zucconi L., Ripa C., Selbmann L., Onofri S. 2002; Effects of UV on the spores of the fungal species Arthrobotrys oligospora and A. ferox . Polar Biol 25:500–505
     [Google Scholar]
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Nitric oxide mediates the fungal-elicitor-enhanced biosynthesis of antioxidant polyphenols in submerged cultures of Inonotus obliquus
Microbiology 155, 3440 (2009); https://doi.org/10.1099/mic.0.030650-0
/content/journal/micro/10.1099/mic.0.030650-0
/content/journal/micro/10.1099/mic.0.030650-0
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