COPPER AMINE OXIDASE1 (CuAO1) of arabidopsis thaliana contributes to abscisic acid-and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction

Molecular Plant

Volumn 4, Issue 4, 2011, Pages 663-678

  Wimalasekera, Rinukshi ^a   Villar, Corina ^a,b   Begum, Tahmina ^a,c   Scherer, Günther F E ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

abscisic acid; COPPER AMINE OXIDASE1; germination; nitric oxide; polyamines; signal transduction

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80051776630     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssr023     Document Type: Article

References (67)

1. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., Carrasco, P., and Tiburcio, A.F. (2010). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta. 231, 1237-1249.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657. (Pubitemid 36927950)
3. An, Z., Jing, W., Liu, Y., and Zhang, W. (2008). Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J. Exp. Bot. 59, 815-825. (Pubitemid 351644661)
4. Angelini, R., Cona, A., Federico, R., Fincato, P., Tavladoraki, P., and Tisi, A. (2010). Plant amine oxidases 'on the move': An update. Plant Physiol. Biochem. 48, 560-564.
5. Bagni, N., and Tassoni, A. (2001). Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids. 20, 301-317. (Pubitemid 32260962)
6. Beligni, M.V., and Lamattina, I. (2000). Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta. 210, 215-221. (Pubitemid 30067885)
7. Besson-Bard, A., Courtoisa, C., Gauthiera, A., Dahana, J., Dobrowolskab, G., Jeandrozc, S., Pugin, A., and Wendehenne, D. (2008a). Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Mol. Plant. 1, 218-228.
8. Besson-Bard, A., Pugin, A., and Wendehenne, D. (2008b). New insights into nitric oxide signaling in plants. Annu. Rev. Plant Biol. 59, 21-39. (Pubitemid 351813022)
9. Bethke, P.C., Gubler, F., Jacobsen, J.V., and Jones, R.L. (2004). Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta. 219, 847-855. (Pubitemid 39282949)
10. Bouchereau, A., Aziz, A., Larher, F., and Martin-Tanguy, J. (1999). Polyamines and environmental challenges: recent development. Plant Sci. 140, 103-125. (Pubitemid 29086551)
11. Bradford, M.M. (1976). A rapid and sensitive method for the quan-titation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochem. 77, 248-254.
12. Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., and Neill, S.J. (2006). ABA inducedNO generation and stomatal closurein Arabidopsis are dependent on H2O2 synthesis. Plant J. 45, 113-122. (Pubitemid 43373736)
13. Chen, C.C., Liang, C.S., Kao, A., and Yang, C. (2009). HHP1 is involved in osmotic stress sensitivity in Arabidopsis. J. Exp. Bot. 60, 1589-1604.
14. Cona, A., Rea, G., Angelini, R., Federico, R., and Tavladoraki, P. (2006). Functions of amine oxidases in plant development and defense. Trends Plant Sci. 11, 80-88. (Pubitemid 43238419)
15. Correa-Aragunde, N., Graziano, M., and Lamattina, L. (2004). Nitric oxide plays a central role in determining lateral root development in tomato. Planta. 218, 900-905. (Pubitemid 38504241)
16. Courtois, C., Besson, A., Dahan, J., Bourque, S., Dobrowolska, G., Pugin, A., and Wendehenne, D. (2008). Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J. Exp. Bot. 59, 155-163. (Pubitemid 351651352)
17. Crawford, N.M. (2006). Mechanisms for nitric oxide synthesis in plants. J. Exp. Bot. 57, 471-478. (Pubitemid 43164378)
18. Cuevas, J.C., Ló pez-Cobollo, R., Alcá zar, R., Zarza, X., Koncz, C., Altabella, T., Salinas, J., Tiburcio, A.F., and Ferrando, A. (2008).Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol. 148, 1094-1105. (Pubitemid 352847555)
19. De Bruxelles, G.L., Peacock, W.J., Dennis, E.S., and Dolferus, R. (1996). Abscisic acid induces the alcohol dehydrogenase gene in Arabidopsis. Plant Physiol. 111, 381-391. (Pubitemid 126640481)
20. Delledonne, M., Xia, Y., Dixon, R.A., and Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature. 394, 585-588. (Pubitemid 28366834)
21. Desikan, R., Cheung, M.-K., Bright, J., Henson, D., Hancock, J.T., and Neill, S. (2004). ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells. J. Exp. Bot. 55, 205-212. (Pubitemid 38119163)
22. Desikan, R., Griffiths, R., Hancock, J., and Neill, S.J. (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, 16314-16318. (Pubitemid 35462792)
23. Galston, A.W., and Kaur-Sawhney, R. (1990). Polyamines in plant physiology. Plant Physiol. 94, 406-410. (Pubitemid 120015568)
24. Galston, A.W., Kaur-Sawhney, R., Altabella, T., and Tiburcio, A.F. (1997). Plant polyamines in reproductive activity and response to abiotic stress. Bot. Acta. 110, 197-207. (Pubitemid 27295513)
25. Gamborg, O.L., Miller, R.A., and Ojima, K. (1968). Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50, 151-158.
26. Gubler, F., Millar, A.A., and Jacobsen, J.V. (2005). Dormancy release, ABA and pre-harvest sprouting. Curr. Opin. Plant Biol.8, 183-187. (Pubitemid 40323548)
27. Guo, F.Q., Okamoto, M., and Crawford, N.M. (2003). Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science. 302, 100-103. (Pubitemid 37210696)
28. He, R., et al. (2004). Nitric oxide represses the Arabidopsis floral transition. Science. 305, 1968-1971.
29. Jaffrey, S.R., and Snyder, S.H. (2001). The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE. 86, p11.
30. Jiang, W., and Yu, D. (2009). Arabidopsis WRKY2 transcription factor mediates seed germination and postgermination arrest of development by abscisic acid. BMC Plant Biol. 9, 96.
31. Kamada-Nobusada, T., Hayashi, M., Fukazawa, M., Sakakibara, H., and Nishimura, M. (2008). A putative peroxisomal polyamine ox-idase, AtPAO4, is involved in polyamine catabolism in Arabidop-sis thaliana. Plant Cell Physiol. 49, 1272-1282.
32. Kojima, H., Hirotani, M., Nakatsubo, N., Kikuchi, K., Urano, Y., Higuchi, T., Hirata, Y., and Nagano, T. (2001). Bioimaging of nitric oxide with fluorescent indicators based on the rhodamine chro-mophore. Anal. Chem. 73, 1967-1973. (Pubitemid 32862401)
33. Kojima, H., Nakatsubo, N., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y., and Nagano, T. (1998). Detection and imaging of nitric oxide with novel fluorescent indicators: diamino-fluoresceins. Anal.Chem. 70, 2446-2453.
34. Koornneef, M., Bentsink, L., and Hilhorst, H. (2002). Seed dormancy and germination. Curr. Opin. Plant Biol. 5, 33-36. (Pubitemid 34060475)
35. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.F., Bloom, R.E., Bodde, S., Jones, J.D.G., and Schroeder, J.I. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis. EMBO J. 22, 2623-2633. (Pubitemid 36712360)
36. Lin, C.C., and Kao, C.H. (2001). Abscisic acid induced changes in cell wall peroxidase activity and hydrogen peroxide level in roots of rice seedlings. Plant Sci. 160, 323-329. (Pubitemid 32109942)
37. Lindermayr, C., Saalbach, G., and Durner, J. (2005). Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 137, 921-930. (Pubitemid 43138164)
38. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real time quantitative PCR and the 2DDCTmethod. Methods. 25, 402-408. (Pubitemid 34164012)
39. Lozano-Juste, J., and Leó n, J. (2010). Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR-and AtNOA1-dependent nitric oxide biosynthesis in Arabi-dopsis. Plant Physiol. 152, 891-903.
40. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410. (Pubitemid 36726490)
41. Moschou, P.N., Paschalidis, K.A., and Roubelakis-Angelakis, K.A. (2008a). Plant polyamine catabolism: the state of the art. Plant Signal. Behav. 3, 1061-1066. (Pubitemid 352847663)
42. Moschou, P.N., Paschalidis, K.A., Delis, I.D., Andriopoulou, A.H., Lagiotis, G.D., Yakoumakis, D.I., and Roubelakis-Angelakis, K.A. (2008b). Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell. 20, 1708-1724. (Pubitemid 352844173)
43. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
44. Negi, S., Santisree, P., Kharshiing, E.V., and Sharma, R. (2010). Inhibition of the ubiquitin-proteasome pathway alters cellular levels of nitric oxide in tomato seedlings. Mol. Plant. 3, 854-869.
45. Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., Morris, P., Ribeiro, D., and Wilson, I. (2008). Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 59, 165-176. (Pubitemid 351651356)
46. Neill, S.J., Desikan, D., Clarke, A., and Hancock, J.T. (2002). Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128, 13-16. (Pubitemid 34115307)
47. Pagnussat, G.C., Simontacchi, M., Puntarulo, S., and Lamattina, L. (2002). Nitric oxide is required for root organogenesis. Plant Physiol. 129, 954-956. (Pubitemid 34801070)
48. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G.J., Grill, E., and Schroeder, J.I. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature. 406, 731-734.
49. Prado, A.M., Colaxco, R., Moreno, N., Silva, A.C., and Feijó, J.A. (2008). Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol. Plant. 1, 703-714.
50. Qiao, W., and Fan, L.-M. (2008). Nitric oxide signalling in plant responses to abiotic stresses. J. Integrative Plant Biol. 50, 1238-1246.
51. Rock, C.D., and Zeevaart, J.A.D. (1991). The aba mutant of Arabi-dopsis thaliana is impaired in epoxy-caretonoid biosynthesis. Proc. Natl Acad. Sci. USA. 88, 7496-7499. (Pubitemid 21915179)
52. Santa-Catarina, C., Silveira, V., Scherer, G.F.E., and Floh, E.I.S. (2007a). Polyamine and nitric oxide levels relate with morphoge-netic evolution in somatic embryogenesis of Ocotea catharinen-sis. Plant Cell Tissue & Organ Culture. 90, 93-101. (Pubitemid 47101242)
53. Santa-Catarina, C., Tun, N.N., Silveira, V., Handro, W., Floh, E.I.S., and Scherer, G.F.E. (2007b). Rapid nitric oxide (NO) release induced by polyamines in tobacco BY-2 cells and Ocotea catharinensis somatic embryos. Plant Cell Tissue & Organ Culture. 90, 93-101.
54. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols. 3, 1101-1108. (Pubitemid 351818697)
55. Silveira, V., Santa-Catarina, C., Tun, N.N., Handro, W., Scherer, G.F.E., Handro, W., Guerra, M., and Floh, E.I.S. (2006). Polyamine effects on the endogenous polyamine contents, nitric oxide release, growth and differentiation of embryonic suspension cultures of Araucaria angustifolia (Bert.) O. Ktze. Plant Sci. 171, 91-98. (Pubitemid 43729702)
56. Tun, N.N., Holk, A., and Scherer, G.F.E. (2001). Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett. 509, 174-176. (Pubitemid 34015937)
57. Tun, N.N., Livaja, M., Kieber, J.J., and Scherer, G.F.E. (2008). Zeatin-induced NO biosynthesis in Arabidopsis seedlings depends on two-component signaling genes. New Phytologist. 178, 515-531. (Pubitemid 351550564)
58. Tun, N.N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., Floh, I.S., and Scherer, G.F.E. (2006). Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 47, 346-354.
59. Walters, D. (2003). Resistance to plant pathogens: possible roles for free polyamines and polyamine catabolism. New Phytologist. 159, 109-115. (Pubitemid 36738343)
60. Wang, P., Du, Y., Li, Y., Ren, D., and Song, C.-P. (2010). Hydrogen peroxide-mediated activation of MAP Kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell. 22, 2981-2998.
61. Wendehenne, D., Pugin, A., Klessig, D.F., and Durner, J. (2001). Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 6, 177-183. (Pubitemid 33145905)
62. Wilson, I.D., Neill, S.J., and Hancock, J.T. (2008). Nitric oxide synthesis and signalling in plants. Plant Cell Env. 31, 622-631. (Pubitemid 351503408)
63. Wimalasekera, R., and Scherer, G.F.E. (2010). Polyamines and cyto-kinin: is nitric oxide biosynthesis the key to overlapping functions? In Nitric Oxide in Plant Physiology, Hayat, S., Mori, M., Pichtel, J., Ahmad, A., eds (Weinheim, Germany: Wiley-Vch), pp. 65-76.
64. Xue, B., Zhang, A., and Jiang, M. (2009). Involvement of polyamine oxidase in abscisic acid-induced cytosolic antioxidant defense in leaves of maize. J. Integr. Plant Biol. 51, 225-234.
65. Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994). A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell. 16, 251-264.
66. Zhang, H., and Forde, B.G. (1998). An Arabidopsis MADS box gene that controls nutrient induced changes in root architecture. Science. 279, 407-409. (Pubitemid 28063380)
67. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). Genvestigator: Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632. (Pubitemid 41071302)