Ultraviolet-B-induced flavonoid accumulation in Betula pendula leaves is dependent upon nitrate reductase-mediated nitric oxide signaling

Tree Physiology

Volumn 31, Issue 8, 2011, Pages 798-807

  Zhang, Ming ^a   Dong, Ju Fang ^b   Jin, Hai Hong ^b   Sun, Li Na ^b   Xu, Mao Jun ^a  

^a HANGZHOU NORMAL UNIVERSITY   (China)

^b ZHEJIANG GONGSHANG UNIVERSITY   (China)

Author keywords

Betula pendula Roth (silver birch); flavonoids; nitrate reductase; nitric oxide; UV B irradiation

Indexed keywords

FLAVONOID; NITRATE REDUCTASE; NITRIC OXIDE;

BIOACCUMULATION; DECIDUOUS TREE; ENZYME ACTIVITY; GENE EXPRESSION; INHIBITOR; LEAF; NITRIC OXIDE; SIGNAL; ULTRAVIOLET B RADIATION;

ARTICLE; BIRCH; ENZYMOLOGY; GENETICS; METABOLISM; PLANT LEAF; RADIATION EXPOSURE; SEEDLING; ULTRAVIOLET RADIATION;

BETULA; FLAVONOIDS; NITRATE REDUCTASE; NITRIC OXIDE; PLANT LEAVES; SEEDLING; ULTRAVIOLET RAYS;

BETULA PENDULA;

EID: 80052594260     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpr070     Document Type: Article

References (75)

1. Bassman, J.H. 2004. Ecosystem consequences of enhanced solar ultraviolet radiation: secondary plant metabolites as mediators of multiple trophic interactions in terrestrial plant communities. Photochem. Photobiol. 79:382-398.
2. Berthke, P.C., M.R. Badger and R.L. Jone. 2004. Apoplastic synthesis of nitric oxide by plant tissue. Plant Cell 16:332-341. (Pubitemid 38192693)
3. Besson-Bard, A., A. Pugin and D. Wendehenne. 2007. New insight into nitric oxide signaling in plants. Annu. Rev. Plant Biol. 59:21-39.
4. Bieza, K. and R. Lois. 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of fa-vonoids and other phenolics. Plant Physiol. 126:1105-1115. (Pubitemid 32656798)
5. Björn, L.O. 1996. Effects of ozone depletion and increased UV-B on terrestrial ecosystems. Int. J. Environ. Stud. 51:217-243. (Pubitemid 27118664)
6. Bradford, M.M. 1976. A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. 2 synthesis. Plant J. 45:113-122. (Pubitemid 43373736)
8. Brown, B.A., C. Cloix, G.H. Jiang, E. Kaiserli, P. Herzyk, J. Daniel, D.J. Kliebenstein and G.I. Jenkins. 2005. A UV-B-specifc signaling component orchestrates plant UV protection. Proc. Natl Acad. Sci. USA 102:18225-1823 0. (Pubitemid 41798529)
9. Caldwell, M.M. 1971. Solar ultraviolet radiation and the growth and development of higher plant. In Photophysiology. Vol 6. Ed. A.C. Giese. Academic Press, New York, pp 131-177.
10. Cantrel, C., T. Vazquez, J. Puyaubert et al. 2011. Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol. 189:415-427.
11. Carimi, F., M. Zottini, A. Costa, I. Cattelan, R. de Michele, M. Terzi and F. Schiavo. 2006. NO signalling in cytokinin-induced programmed cell death. Plant, Cell Environ. 28:1171-1178.
12. Cerovic, Z.G., A. Ounis, A. Cartelat, G. Latouce, Y. Goulas, S. Meyer and I. Moya. 2002. The use of chlorophyll fuorescence excitation spectra for the non-destructive in situ assessment of UV-absorbing compounds in leaves. Plant, Cell Environ. 25:1663-1676. (Pubitemid 35456650)
13. Clarke, G.M. and T.N. Higgins. 2000. Laboratory investigation of hemo-globinopathies and thalassemias: review and update. Clin. Chem. 46:1284-1290. (Pubitemid 30643300)
14. Corpas, F.J., J.B. Barroso, A. Carreras, M. Quirós, A.M. León, M.C. Romero-Puertas and F.J. Esteban. 2004. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol. 136:2722-2733. (Pubitemid 41071311)
15. Corpas, F.J., M. Chaki, A. Fernández-Ocaña, R. Valderrama, J.M. Palma and A. Carreras. 2008. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 49:1711-1722.
16. Crawford, N.M., M. Galli, R. Tischner, Y.M. Heimer, M. Okamoto and A. Mack. 2006. Response to Zemojtel et al.: Plant nitric oxide syn-thase: back to square one. Trends Plant Sci. 11:526-527. (Pubitemid 44636299)
17. Dean, J.V. and J.E. Harper. 1988. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol. 88:389-395.
18. Desikan, R., R. Griffths, J.T. Hancock and S.J. Neill. 2002. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 99:16314-16319.
19. Durner, J. and D.F. Klessig. 1999. Nitric oxide as a signal in plants. Curr. Opin. Plant Biol. 2:369-374. (Pubitemid 29464062)
20. Flores-Pérez, U., S. Sauret-Güeto, E. Gas, P. Jarvis and M. Rodríguez-Concepción. 2008. A mutant impaired in the production of plas-tome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant C e ll 20:130 3-1315.
21. Frohnmeyer, H. and D. Staiger. 2003. Ultraviolet-B radiation-mediated responses in plants, balancing damage and protection. Plant Physiol. 133:142 0-14 2 8. (Pubitemid 38047273)
22. Furchgott, R.F. 1995. Special topics: nitric oxide. Annu. Rev. Physiol. 57:659-682.
23. Guo, F.Q., M. Okamoto and N.M. Crawford. 2003. Identifcation of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:10 0-103.
24. Gupta, K.J. and W.M. Kaiser. 2010. Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol. 51:576-584.
25. Gupta, K.J., A.R. Fernie, W.M. Kaiser and J.T. van Dongen. 2011a. On the origins of nitric oxide. Trends Plant Sci. 16:160-168.
26. Gupta, K.J., D. Hincha and L.A.J. Mur. 2011b. NO way to treat a cold. New Phytol. 189:360-363.
27. Hahlbrock, K., P. Bednarek, I. Ciolkowski et al. 2003. Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions. Proc. Natl Acad. Sci. USA 10 0:1456 9-14576. (Pubitemid 37499283)
28. Hao, G., X. Du, F. Zhao, R. Shi and J. Wang. 2009. Role of nitric oxide in UV-B-induced activation of PAL and stimulation of favonoid biosynthesis in Ginkgo biloba callus. Plant Cell Tiss. Org. Cult. 97:175-185.
29. He, J.M., H. Xu, X.P. She, X.G. Song and W.M. Zhao. 2005. The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Funct. Plant Biol. 32:237-247. (Pubitemid 40689809)
30. Hertog, M.G.L., P.C.H. Hollman and M.B. Katan. 1992. Content of potentially anticarcinogenic favonoids of 28 vegetables and 9 fruits commonly consumed in The Netherlands. J. Agric. Food Chem. 40:2379-2383.
31. Ingestad, T. 1962. Macroelement nutrition of pine, spruce and birch seedlings in nutrient solutions. Medd. Statens Skogsforskningsinst. 51:16-21.
32. Jansen, M.A.K., V. Gaba and B.M. Greenberg. 1998. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends P la n t S c i. 3:131-135. (Pubitemid 28187199)
33. Jasid, S., M. Simontacchi, C.G. Bartoli and S. Puntarulo. 2006. Chloroplasts as a nitric oxide cellular source: effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol. 142:124 6-1255.
34. Jordan, B.R. 1996. The effects of UV-B radiation on plants: a molecular perspective. Adv. Bot. Res. 22:97-162. (Pubitemid 2623830)
35. Jordan, B.R. 2002. Molecular response of plant cells to UV-B stress. Funct. Plant Biol. 29:909-916. (Pubitemid 34949475)
36. Kotilainen, T., T. Venäläinen, R. Tegelberg, A. Lindfors, R. Julkunen-Tiitto, S. Sutinen, R.B. O'Hara and P.J. Aphalo. 2009. Assessment of biological spectral weighting functions for phenolic metabolites and growth responses in silver birch seedlings. Photochem. Photobiol. 8 5:13 4 6-135 5.
37. Landry, L., C. Chapple and R. Last. 1995. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxida-tive damage. Plant Physiol. 109:1159-1166. (Pubitemid 3020286)
38. Li, J., T.M. Ou-Lee, R. Raba, R.G. Amundson and R.L. Last. 1993. Arabidopsis favonoid mutants are hypersensitive to UV-B irradiation. P la n t C e ll 5:171-17 9.
39. -▲▲CT method. Methods 25:402-408. (Pubitemid 34164012)
40. Lozano-Juste, J. and J. Leon. 2010. Enhanced abscissic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR-and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 152:891-903.
41. Mattila, P., J. Astola and J. Kumpulainen. 2000. Determination of favo-noids in plant material by HPLC with diode-array and electro-array detections. J. Agric. Food Chem. 48:5834-5841. (Pubitemid 32056815)
42. Modolo, L.V., O. Augusto, I.M.G. Almeida, C.A.F. Pinto-Maglio, H.C. Oliveira, K. Seligman and L. Salgado. 2006. Decreased arginine and nitrite levels in nitrate reductase-defcient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Sci. 171:34-40. (Pubitemid 44251004)
43. Morales, L.O., R. Tegelberg, M. Brosche, M. Keinanen, A. Lindfors and R.J. Aphalo. 2010. Effects of solar UV-A and UV-B radiation on gene expression and phenolic accumulation in Betula pendula leaves. Tree Physiol. 30:923-934.
44. Moreau, M., G.I. Lee, Y. Wang, B.R. Crane and D.F. Klessig. 2008. AtNOS/A1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. J. Biol. Chem. 283:32957-32967.
45. Murphy, M.E. and E. Noack. 1994. Nitric oxide assay using hemoglobin method. Methods Enzymol. 233:240-250.
46. Neill, S.J., R. Desikan and J.T. Hancock. 2003. Nitric oxide signaling in plants. New Phytol. 159:11-22.
47. Pasqualini, S., S. Meier, C. Gehring, L. Madeo, M. Fornaciari, B. Romano and L. Ederli. 2009. Ozone and nitric oxide induce cGMP-dependent and-independent transcription of defense genes in tobacco. New Phytol. 181:860-870.
48. Qu, Y., H. Feng, Y. Wang, M. Zhang, J. Cheng, X. Wang and L. An. 2006. Nitric oxide functions as a signal in ultraviolet-B induced inhibition of pea stems elongation. Plant Sci. 170:994-1000. (Pubitemid 43378996)
49. Rockel, P., F. Strube, A. Rockel, J. Wildt and W.M. Kaiser. 2002. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53:103-110. (Pubitemid 34043147)
50. Rozema, J., J. van de Staaij, L.O. Björn and M. Caldwell. 1997. UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol. Evol. 12:22-28.
51. Rumer, S., K.J. Gupta and W.M. Kaiser. 2009. Plant cells oxidize hydrox-ylamines to NO. J. Exp. Bot. 60:2065-2072.
52. Salgado, I., L.V. Modolo, O. Augusto, M.R. Braga and H.C. Oliveira. 2007. Mitochondrial nitric oxide synthesis during plant-pathogen interactions: role of nitrate reductase in providing. Plant Cell Monographs 5:237-254.
53. Scheible, W.R., M. Lauerer, E.D. Schulze, M. Caboche and M. Stitt. 1997. Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J. 11:671-691. (Pubitemid 27206978)
54. Tian, Q.Y., D.H. Sun, M.G. Zhao and W.H. Zhang. 2007. Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos L. New Phytol. 174:322-331.
55. Tossi, V., L. Lamattina and R. Cassia. 2009. An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol. 181:871-879.
56. Tun, N. 2001. Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett. 509:174-176. (Pubitemid 34015937)
57. Tun, N.N., C. Santa-Catarina, T. Begum, V. Silveira, W. Handro, E.I.S. Floh and G.F.E. Scherer. 2006. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 47:346-354.
58. Ulm, R. and F. Nagy. 2005. Signalling and gene regulation in response to UV light. Curr. Opin. Plant Biol. 8:477-482. (Pubitemid 41188180)
59. Wang, J.W., L.P. Zheng and R.X. Tan. 2007. Involvement of nitric oxide in cerebroside-induced defense responses and taxol production in Taxus yunnanensis suspension cells. Appl. Microbiol. Biotechnol. 7 5:118 3-119 0. (Pubitemid 46944547)
60. Wilkinson, J.Q. and N.M. Crawford. 1993. Identifcation and characterization of chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes N I A1 and NIA2. Mol. Gen. Genet. 239:289-297. (Pubitemid 23167510)
61. Wilson, I.D., S.J. Neill and J.T. Hancock. 2008. Nitric oxide synthesis and signaling in plants. Plant, Cell Environ. 31:622-631. (Pubitemid 351503408)
62. Xu, M.J. 2007. Nitric oxide: a potential key point of the signaling network leading to plant secondary metabolite biosynthesis. Prog. Nat. Sci. 12:1397-1404.
63. Xu, M.J. and J.F. Dong. 2005. Elicitor-induced nitric oxide burst is essential for triggering catharanthine synthesis in Catharanthus roseus suspension cells. Appl. Microbiol. Biotechnol. 67:40-44.
64. Xu, M.J. and J.F. Dong. 2008. Synergistic action between jasmonic acid and nitric oxide in inducing matrine accumulation of Sophora flave-scens suspension cells. J. Integr. Plant Biol. 50:91-100.
65. Xu, M.J., J.F. Dong and M.Y. Zhu. 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.
66. Xu, M.J., J.F. Dong and X.B. Zhang. 2008. Signal interaction between nitric oxide and hydrogen peroxide in heat shock-induced hypericin production of Hypericum perforatum suspension cells. Sci. Chin. Ser. C: Life Sci. 8:676-686.
67. Yamamoto, A., S. Katou, H. Yoshioka, N. Doke and K. Kawakita. 2003. Nitrate reductase, a nitric oxide-producing enzyme: induction by pathogen signals. J. Gen. Plant Pathol. 69:218-229.
68. Yamasaki, H. 2000. Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibi-tion in vivo. Philos. Trans. R Soc. Lond. B Biol. Sci. 355:1477-1488.
69. Yamasaki, H., Y. Sakihama and S. Takahashi. 1999. An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 4:128-129. (Pubitemid 29178026)
70. Yao, L., Y. Jiang, B. D'Arcy, R. Singanusong, N. Datta, N. Caffn, and K. Raymont. 2004. Quantitative high-performance liquid chromatogra-phy analyses of favonoids in australian Eucalyptus honeys. J. Agric. Food Chem. 52:210-214.
71. Yu, X., S. Sukumaran and L. Márton. 1998. Differential expression of the Arabidopsis Nia1 and Nia2 genes. Plant Physiol. 116:1091-1096.
72. Zemojtel, T., A. Fröhlich, M.C. Palmieri, M. Kolanczyk, I. Mikula and L.S. Wyrwicz. 2006. Plant nitric oxide synthase: a never-ending story? Trends Plant Sci. 11:524-525. (Pubitemid 44636300)
73. Zhao, J., L.C. Davis and R. Verpoorte. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 23:283-333. (Pubitemid 40560881)
74. Zhao, M.G., L. Chen, L.L. Zhang and W.H. Zhang. 2009. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 151:755-767.
75. Zheng, L.P., Y.T. Guo, J.W. Wang and R.X. Tan. 2008. Nitric oxide potentates oligosaccharide-induced artemisinin production in Artemisia annua hairy roots. J. Integr. Plant Biol. 50:49-55.