Ozone induces flavonol production of Ginkgo biloba cells dependently on nitrate reductase-mediated nitric oxide signaling

Environmental and Experimental Botany

Volumn 75, Issue , 2012, Pages 114-119

  Xu, Maojun ^a   Zhu, Yun ^b   Dong, Jufang ^b   Jin, Haihong ^a,b   Sun, Lina ^a,b   Wang, Zhian ^c   Lu, Zhonghua ^c   Zhang, Ming ^a   Lu, Dan ^a  

^a HANGZHOU NORMAL UNIVERSITY   (China)

^b ZHEJIANG GONGSHANG UNIVERSITY   (China)

^c Zhejiang Research Institute of Traditional Chinese Medicine   (China)

Author keywords

Flavonol; Flavonol accumulation; Ginkgo biloba cells; Nitrate reductase (NR); Nitric oxide (NO); Ozone; Ozone tolerance

Indexed keywords

BIOACCUMULATION; ENZYME ACTIVITY; GYMNOSPERM; INHIBITOR; NITRATE; NITRIC OXIDE; OZONE; PHYTOCHEMISTRY; PIGMENT; POLLUTION EXPOSURE; POLLUTION TOLERANCE; SECONDARY METABOLITE; INHIBITION;

GINKGO BILOBA;

EID: 81555214706     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2011.09.005     Document Type: Article

References (53)

1. Arasimowicz M., Floryszak-Wieczorek J. Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci. 2007, 172:876-887.
2. Betz G.A., Knappe C., Lapierre C., Olbrich M., Welzl G., Langebartels C., Heller W., Sandermann H., Ernst D. Ozone affects shikimate pathway transcripts and monomeric lignin composition in European beech (Fagus sylvatica L.). Eur. J. Forest Res. 2009, 128:109-116.
3. Blande J.D., Tiiva P., Oksanen E., Holopainen J.K. Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula×tremuloides) clones under ambient and elevated ozone concetrations in the field. Global Change Biol. 2007, 13:2538-2550.
4. Booker F.L., Muntifering R., McGrath M., Burkey K.O., Decoteau D., Fiscus E.L., Manning W., Krupa S., Chappelka A., Grantz D.A. The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. J. Integr. Plant Biol. 2009, 51:337-351.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
6. Byvoet P., Balis J.U., Shelley S.A., Montgomery M.R., Barber M.J. Detection of hydroxyl radicals upon interaction of ozone with aqueous media or extracellular surfactant: the role of trace iron. Arch. Biochem. Biophys. 1995, 319:464-469.
7. Cabané M., Pireaux J-C., Léger E., Weber E., Dizengremel P., Pollet B., Lapierre C. Condensed lignins are synthesized in poplar leaves exposed to zone. Plant Physiol. 2004, 134:586-594.
8. Carimi F., Zottini M., Costa A., Cattelan I., de Michele R., Terzi M., Schiavo F. NO signalling in cytokinin-induced programmed cell death. Plant Cell Environ. 2006, 28:1171-1178.
9. Clarke G.M., Higgins T.N. Laboratory investigation of hemoglobinopathies and thalassemias: review and update. Clin. Chem. 2000, 46:1284-1290.
10. Corpas F.J., Chaki M., Fernandez-Ocana A., Valderrama R., Palma J.M., Carreras A., Begara-Morales J.C., Airaki M., del Rio L.A., Barroso J.B. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 2008, 49:1711-1722.
11. Dean J.V., Harper J.E. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol. 1988, 88:389-395.
12. Delledonne M., Xia Y.J., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature 1998, 394:585-588.
13. Dubber M.J., Sewram V., Mshicileli N., Shephard G.S., Kanfer I. The simultaneous determination of selected flavonol glycosides and aglycones in Ginkgo biloba oral dosage forms by high-performance liquid chromatography-electrospray ionization-mass spectrometry. J. Pharm. Biomed. Anal. 2005, 37(4):723-731.
14. Ederli L., Morettini R., Borgogni A., Wasternack C., Miersch O., Reale L., Ferranti F., Tosti N., Pasqualini S. Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol. 2006, 142:595-608.
15. Foy D., Lee E.H., Rowland R., Devine T.E., Buzzel R.I. Ozone tolerance related to flavonol glycoside genes in soybean. J. Plant Nutr. 1995, 18:637-647.
16. Furchgott R.F. Special topics: nitric oxide. Annu. Rev. Physiol. 1995, 57:659-682.
17. Gould K.S., Lamotte O., Klinguer A., Pugin A., Wendehenne D. Nitric oxide production in tobacco leaf cells: a generalized stress response?. Plant Cell Environ. 2003, 26:1851-1862.
18. Hahlbrock K., Bednarek P., Ciolkowski I., Hamberger B., Heise A., Liedgens H., Logemann E., Nürnberger T., Schmelzer E., Somssich I.E., Tan J. Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14569-14576.
19. Heath R.L. The biochemistry of ozone attack on the plasma membrane of plant cells. Recent Adv. Phytochem. 1987, 21:29-54.
20. Heath R.L., Taylor G.E. Physiological processes and plant responses to ozone exposure. Forest Decline and Ozone 1997, 317-368. Springer-Verlag, Berlin/Heidelberg. H. Sandermann, A.R. Wellburn, R.L. Heath (Eds.).
21. IPCC Summary for policymakers. Report of Working Group I. Intergovernmental Panel on Climate Change 2001.
22. Janzik I., Preiskowski S., Kneifel H. Ozone has dramatic effects on the regulation of the prechorismate pathway in tobacco (Nicotiana tabacum L. cv. Bel W3). Planta 2005, 223:20-27.
23. Krupa S.V., Manning W.J. Atmospheric ozone: formation and effects on vegetation. Environ. Pollut. 1988, 50:101-137.
24. Langebartels C., Kangasjärvi J. Ethylene and jasmonate as regulators of cell death in disease resistance. Molecular Ecotoxicology of Plants 2004, 75-109. Springer-Verlag, Berlin/Heidelberg. H. Sandermann (Ed.).
25. Langebartels C., Schraudner M., Heller W., Ernst D., Sandermann H. Oxidative stress and defense reactions in plants exposed to air pollutants and UV-B radiation. Oxidative Stress in Plants 2002, 105-135. Taylor and Francis, London. D. Inze, M. Van Montagu (Eds.).
26. Lozano-Juste J., Leon J. Enhanced abscissic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 2010, 152:891-903.
27. Lu D., Dong J., Jin H., Sun L., Xu X., Zhou T., Zhu Y., Xu M. Nitrate reductase-mediated nitric oxide generation is essential for fungal elicitor-induced camptothecin accumulation of Camptotheca acuminata suspension cell cultures. Appl. Microbiol. Biotechnol. 2011, 90:1073-1081.
28. Mehlhorn H., Tabner B.J., Wellburn A.R. Electron spin resonance evidence for the formation of free radicals in plants exposed to ozone. Nature 1990, 327:417-418.
29. Murashige T., Skoog F. A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol. Plant 1962, 15:473-497.
30. Murphy M.E., Noack E. Nitric oxide assay using hemoglobin method. Methods Enzymol. 1994, 233:240-250.
31. Neill S., Barros R., Bright J., Desikan R., Hancock J., Harrison J., Morris P., Ribeiro D., Wilson I. Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 2008, 59:165-176.
32. Pasqualini S., Meier S., Gehring C., Madeo L., Fornaciari M., Romano B., Ederli L. Ozone and nitric oxide induce cGMP-dependent and-independent transcription of defence genes in tobacco. New Phytol. 2009, 181:860-870.
33. Pell E.J., Schlagnhaufer C.D., Arteca R.N. Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol. Plant 1997, 100:264-273.
34. Richter C.A., Wild A. Phenolic compounds in needles of Norway spruce trees in relation to novel forest declines I. Studies on trees from a site in the northern Black Forest. Biochem. Physiol. Pflanzen 1988, 188:305-320.
35. Rockel P., Strube F., Rockel A., Wildt J., Kaiser W.M. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 2002, 53:103-110.
36. Rozema J., van de Staaij J., Bjorn L.O., Caldwell M. UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol. Evol. 1997, 12:22-28.
37. Salgado I., Modolo L.V., Augusto O., Braga M.R., Oliveira H.C. Mitochondrial nitric oxide synthesis during plant-pathogen interactions: role of nitrate reductase in providing. Plant Cell Monogr. 2007, 5:237-254.
38. Sandermann H., Ernst D., Heller W., Langebartels C. Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci. 1998, 3:47-50.
39. Scheible W.R., Lauerer M., Schulze E.D., Caboche M., Stitt M. Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J. 1997, 11:671-691.
40. Sharma Y.K., Davis K.R. The effects of ozone on antioxidant responses in plants. Free Radic. Biol. Med. 1997, 23(3):480-488.
41. Tossi V., Lamattina L., Cassia R. An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol. 2009, 181(4):871-879.
42. Tun N. Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett. 2001, 509(2):174-176.
43. Wang J.W., Zheng L.P., Tan R.X. Involvement of nitric oxide in cerebroside-induced defense responses and taxol production in Taxus yunnanensis suspension cells. Appl. Microbiol. Biotechnol. 2007, 75:1183-1190.
44. Wu S.J., Qi J.L., Zhang W.J., Liu S.H., Xiao F.H., Zhang M.S., Xu G.H., Zhao W.G., Shi M.W., Pang Y.J., Shen H.G., Yang Y.H. Nitric Oxide Regulates Shikonin Formation in Suspension-Cultured Onosma paniculatum Cells. Plant Cell Physiol. 2009, 50:118-128.
45. Xu M.J. Nitric oxide: a potential key point of the signaling network leading to pant secondary metabolite biosynthesis. Prog. Nat. Sci. 2007, 17:1397-1404.
46. Xu M.J., Dong J., Wang H., Huang L. Complementary action of jasmonic acid on salicylic acid in mediating fungal elicitor-induced flavonol glycoside accumulation of Ginkgo biloba cells. Plant Cell Environ. 2009, 32:960-967.
47. Xu M.J., Dong J., Zhu M. Nitric oxide mediates the fungal elicitor-induced hypericin production of hypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiol. 2005, 139:991-998.
48. Yamamoto A., Katou S., Yoshioka H., Doke N., Kawakita K. Nitrate reductase, a nitric oxide-producing enzyme: induction by pathogen signals. J. Gen. Plant Pathol. 2003, 69:218-229.
49. Yamamoto-Katou A., Katou S., Yoshioka H., Doke N., Kawakita K. Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant Cell Physiol. 2006, 47:726-735.
50. 2. Plant Physiol. 1997, 115:1405-1412.
51. Yamasaki H., Sakihama Y., Takahashi S. An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 1999, 4:128-129.
52. Zhao M.G., Chen L., Zhang L.L., Zhang W.H. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 2009, 151:755-767.
53. Zheng L.P., Guo Y.T., Wang J.W., Tan R.X. Nitric oxide potentiates oligosaccharide-induced artemisinin production in Artemisia annua hairy roots. J. Integr. Plant Biol. 2008, 50:49-55.