Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. Falcata that confers cold tolerance through up-regulating polyamine oxidation

Plant Biotechnology Journal

Volumn 12, Issue 5, 2014, Pages 601-612

  Guo, Zhenfei ^a   Tan, Jiali ^a   Zhuo, Chunliu ^a   Wang, Congying ^a   Xiang, Bin ^a   Wang, Zengyu ^b  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b PLANT BIOLOGY DIVISION   (United States)

Author keywords

Cold tolerance; Polyamine oxidation; S adenosylmethionine synthetase

Indexed keywords

MEDICAGO SATIVA; MEDICAGO SATIVA SUBSP. FALCATA; NICOTIANA TABACUM;

ABSCISIC ACID; ANTIOXIDANT; ETHYLENE; ETHYLENE DERIVATIVE; HYDROGEN PEROXIDE; MESSENGER RNA; METHIONINE ADENOSYLTRANSFERASE; NITRIC OXIDE; OXIDOREDUCTASE; POLYAMINE; POLYAMINE OXIDASE; S ADENOSYLMETHIONINE;

ACCLIMATIZATION; ADAPTATION; ALFALFA; COLD; DRUG EFFECTS; ENZYMOLOGY; FREEZING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; NUCLEIC ACID HYBRIDIZATION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME; TOBACCO; TRANSGENIC PLANT; UPREGULATION;

ABSCISIC ACID; ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ANTIOXIDANTS; CLONING, MOLECULAR; COLD TEMPERATURE; ETHYLENES; FREEZING; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; MEDICAGO SATIVA; METHIONINE ADENOSYLTRANSFERASE; NITRIC OXIDE; NUCLEIC ACID HYBRIDIZATION; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PLANTS, GENETICALLY MODIFIED; POLYAMINES; RNA, MESSENGER; S-ADENOSYLMETHIONINE; SIGNAL TRANSDUCTION; TIME FACTORS; TOBACCO; UP-REGULATION;

EID: 84901621248     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12166     Document Type: Article

References (65)

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. Alcázar, R., Cuevas, J.C., Planas, J., Zarza, X., Bortolotti, C., Carrasco, P., Salinas, J., Tiburcio, A.F. and Altabella, T. (2011) Integration of polyamines in the cold acclimation response. Plant Sci. 180, 31-38.
3. Asada, K. (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639.
4. Boerjan, W., Bauw, G., Van Montagu, M. and lnzé, D. (1994) Distinct phenotypes generated by overexpression and suppression of S-adenosyl-L-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell, 6, 1401-1414.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Capell, T., Bassie, L. and Christou, P. (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl Acad. Sci. USA, 101, 9909-9914.
7. Christmann, A., Moes, D., Himmelbach, A., Yang, Y., Tang, Y. and Grill, E. (2006) Integration of abscisic acid signalling into plant responses. Plant Biol. 8, 314-325.
8. Cona, A., Rea, G., Angelini, R., Federico, R. and Tavladoraki, P. (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci. 11, 80-88.
9. Cuevas, J.C., Lopez-Cobollo, R., Alcazar, 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 ABA levels in response to low temperature. Plant Physiol. 148, 1094-1105.
10. Foyer, C.H. and Noctor, G. (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17, 1866-1875.
11. Gonzalez, M.E., Marco, F., Minguet, E.G., Carrasco-Sorli, P., Blázquez, M.A., Carbonell, J., Ruiz, O.A. and Pieckenstain, F.L. (2011) Perturbation of spermine synthase gene expression and transcript profiling provide new insights on the role of the tetraamine spermine in Arabidopsis defense against Pseudomonas viridiflava. Plant Physiol. 156, 2266-2277.
12. Good, X., Kellogg, J.A., Wagoner, W., Langhoff, D., Matsumura, W. and Bestwick, R.K. (1994) Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase. Plant Mol. Biol. 26, 81-90.
13. Goto, D.B., Ogi, M., Kijima, F., Kumagai, T., Werven, F.V., Onouchi, H. and Naito, S. (2002) A single-nucleotide mutation in a gene encoding S-adenosylmethionine synthetase is associated with methionine over-accumulation phenotype in Arabidopsis thaliana. Genes Genet. Syst. 77, 89-95.
14. Grossmann, K., Häuser, C., Sauerbrey, E., Fritsch, H., Schmidt, O. and Jung, J. (1989) Plant growth retardants as inhibitors of ethylene production. J. Plant Physiol. 134, 538-543.
15. Gupta, K., Dey, A. and Gupta, B. (2013) Plant polyamines in abiotic stress responses. Acta Physiol. Plant. 35, 2015-2036.
16. Jiang, M. and Zhang, J. (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and upregulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 53, 2401-2410.
17. Kasinathan, V. and Wingler, A. (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol. Plant. 121, 101-107.
18. Kasukabe, Y., He, L., Nada, K., Misawa, S., Ihara, I. and Tachibana, S. (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stress and upregulates the expression of various stress regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol. 45, 712-722.
19. Kasukabe, Y., He, L., Watakabe, Y., Otani, M., Shimada, T. and Tachibana, S. (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotech. 23, 75-83.
20. Kusano, T., Berberich, T., Tateda, C. and Takahashi, Y. (2008) Polyamines: essential factors for growth and survival. Planta, 228, 367-381.
21. Lee, J.-H., Chae, H.S., Lee, J.-H., Hwang, B., Hahn, K.W., Kang, B.G. and Kim, W.T. (1997) Structure and expression of two cDNAs encoding S-adenosyl-L-methionine synthetase of rice (Oryza sativa L.). Biochim. Biophys. Acta, 1354, 13-18.
22. Li, W., Han, Y., Tao, F. and Chong, K. (2011) Knockdown of SAMS genes encoding S-adenosyl-l-methionine synthetases causes methylation alterations of DNAs and histones and leads to late flowering in rice. J. Plant Physiol. 168, 1837-1843.
23. Lindroth, A.M., Saarikoski, P., Flygh, G., Clapham, D., Gronroos, R., Thelander, M., Ronne, H. and von Arnold, S. (2001) Two S-adenosylmethionine synthetase-encoding genes differentially expressed during adventitious root development in Pinus contorta. Plant Mol. Biol. 46, 335-346.
24. Miller, G., Suzuki, N., Ciftci-Yilmaz, S. and Mittler, R. (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ. 33, 453-467.
25. Mitsuya, Y., Takahashi, Y., Berberich, T., Miyazaki, A., Matsumura, H., Takahashi, H., Terauchi, R. and Kusano, T. (2009) Spermine signaling plays a significant role in the defense response of Arabidopsis thaliana to cucumber mosaic virus. J. Plant Physiol. 166, 626-643.
26. 2 signatures that direct tolerance responses in tobacco. Plant Cell, 20, 1708-1724.
27. Moschou, P.N., Paschalidis, K.A. and Roubelakis-Angelakis, K.A. (2008b) Plant polyamine catabolism: the start of the art. Plant Signal Behav. 3, 1061-1066.
28. Moschou, P.N., Sarris, P.F., Skandalis, N., Andriopoulou, A.H., Paschalidis, K.A., Panopoulos, N.J. and Roubelakis-Angelakis, K.A. (2009) Engineered polyamine catabolism preinduces tolerance of tobacco to bacteria and oomycetes. Plant Physiol. 149, 1970-1981.
29. Moschou, P.N., Wu, J., Cona, A., Tavladoraki, P., Angelini, R. and Roubelakis-Angelakis, K.A. (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J. Exp. Bot. 63, 5003-5015.
30. Murray, M.G. and Thompson, W.F. (1980) Rapid isolation of high molecular weight DNA. Nucleic Acids Res. 8, 4321-4325.
31. Nambeesan, S., AbuQamar, S., Laluk, K., Mattoo, A.K., Mickelbart, M.V., Ferruzzi, M.G., Mengiste, T. and Handa, A.K. (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol. 158, 1034-1045.
32. 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.
33. Pang, C., Wang, C., Chen, H., Guo, Z. and Li, C. (2009) Transcript profiling of cold responsive genes in Medicago falcata. In Molecular Breeding of Forage and Turf (Yamada, T. and Spangenberg, G., eds), pp. 141-149. Netherlands: Springer.
34. Parra-Lobato, M.C. and Gomez-Jimenez, M.C. (2011) Polyamine-induced modulation of genes involved in ethylene biosynthesis and signalling pathways and nitric oxide production during olive mature fruit abscission. J. Exp. Bot. 62, 4447-4465.
35. Pennycooke, J.C., Cheng, H. and Stockinger, E.J. (2008) Comparative genomic sequence and expression analyses of Medicago truncatula and alfalfa subspecies falcata COLD-ACCLIMATION-SPECIFIC genes. Plant Physiol. 146, 1242-1254.
36. Pulla, R.K., Kim, Y.-J., Parvin, S., Shim, J.-S., Lee, J.-H., Kim, Y.-J., In, J.-G., Senthil, K.S. and Yang, D.-C. (2009) Isolation of S-adenosyl-L-methionine synthetase gene from Panax ginseng C.A. meyer and analysis of its response to abiotic stresses. Physiol. Mol. Biol. Plants. 15, 267-275.
37. Qi, Y.-C., Wang, F.-F., Zhang, H. and Liu, W.-Q. (2010) Overexpression of Suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco. Acta Physiol. Plant. 32, 263-269.
38. 2 and ethylene is involved in cotton fiber cell elongation by modulating ROS homeostasis. Plant Signal Behav. 3, 194-196.
39. Rea, G., de Pinto, M.C., Tavazza, R., Biondi, S., Gobbi, V., Ferrante, P., De Gara, L., Federico, R., Angelini, R. and Tavladoraki, P. (2004) Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant Physiol. 134, 1414-1426.
40. Rodríguez, A.A., Maiale, S.J., Menéndez, A.B. and Ruiz, O.A. (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J. Exp. Bot. 60, 4249-4262.
41. Roy, M. and Wu, R. (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci. 160, 869-875.
42. Roy, M. and Wu, R. (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci. 163, 987-992.
43. Rzewuski, G., Cornell, K.A., Rooney, L., Bürstenbinder, K., Wirtz, M., Hell, R. and Sauter, M. (2007) OsMTN encodes a 5'-methylthioadenosine nucleosidase that is up-regulated during submergence-induced ethylene synthesis in rice (Oryza sativa L.). J. Exp. Bot. 58, 1505-1514.
44. Sánchez-Aguayo, I., Rodríguez-Galán, J.M., García, R., Torreblanca, J. and Pardo, J.M. (2004) Salt stress enhances xylem development and expression of S-adenosyl-L-methionine synthase in lignifying tissues of tomato plants. Planta, 220, 278-285.
45. Shen, B., Li, C. and Tarczynski, M.C. (2002) High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S-adenosyl-L-methionine synthetase 3 gene. Plant J. 29, 371-380.
46. Slocum, R.D., Flores, H.E., Gaiston, A.W. and Weinstein, L.H. (1989) Improved method for HPLC analysis of polyamines, agmatine and aromatic monoamines in plant tissue. Plant Physiol. 89, 512-517.
47. Suzuki, N. and Mittler, R. (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol. Plant. 126, 45-51.
48. Tabuchi, T., Kawaguchi, Y., Azuma, T., Nanmori, T. and Yasuda, T. (2005) Similar regulation patterns of choline monooxygenase, phosphoethanolamine N-methyltransferase and S-adenosyl-L-methionine synthetase in leaves of the halophyte Atriplex nummularia L. Plant Cell Physiol. 46, 505-513.
49. Tabuchi, T., Okada, T., Takashima, Y., Azuma, T., Nanmori, T. and Yasuda, T. (2006) Transcriptional response of glycinebetaine-related genes to salt stress and light in leaf beet. Plant Biotech. 23, 317-320.
50. Tan, J., Wang, W., Xiang, B., Han, R. and Guo, Z. (2013a) Hydrogen peroxide and nitric oxide mediated cold- and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant, Cell Environ. 36, 288-299.
51. Tan, J., Zhuo, C. and Guo, Z. (2013b) Nitric oxide mediates cold- and dehydration-induced expression of a novel MfHyPRP that confers tolerance to abiotic stress. Physiol. Plant. 149, 310-320.
52. Tiburcio, A.F., Kaur-Sawhney, R., Ingersoll, R.B. and Galston, A.W. (1985) Correlation between polyamines and pyrrolidine alkaloids in developing tobacco callus. Plant Physiol. 78, 323-326.
53. 2. Physiol. Plant. 136, 30-44.
54. Wi, S.J., Kim, W.T. and Park, K.Y. (2006) Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Rep. 25, 1111-1121.
55. Wimalasekera, R., Villar, C., Begum, T. and Scherer, G.F.E. (2011) COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol. Plant 4, 663-678.
56. 2+-permeable channels and pollen tube growth. Plant J. 63, 1042-1053.
57. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Miyazaki, A., Takahashi, T., Michael, A. and Kusano, T. (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett. 22, 6783-6788.
58. Yoda, H., Yamaguchi, Y. and Sano, H. (2003) Induction of hypersensitive response by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol. 132, 1973-1981.
59. Yoda, H., Hiroi, Y. and Sano, H. (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol. 142, 193-206.
60. Zago, E., Morsa, S., Dat, J.F., Alard, P., Ferrarini, A., Inzé, D., Delledonne, M. and Van Breusegem, F. (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol. 141, 404-411.
61. Zhang, A., Jiang, M., Zhang, J., Tan, M. and Hu, X. (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol. 141, 475-487.
62. Zhang, A., Jiang, M., Zhang, J., Ding, H., Xu, S., Hu, X. and Tan, M. (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol. 175, 36-50.
63. 2 and NO production and antioxidant defences. Plant, Cell Environ. 32, 509-519.
64. Zhang, L., Zhao, M., Qiu, Y., Tian, Q. and Zhang, W. (2011) Comparative studies on tolerance of Medicago truncatula and Medicago falcata to freezing. Planta, 234, 445-457.
65. Zhuo, C., Wang, T., Lu, S., Zhao, Y., Li, X. and Guo, Z. (2013) A cold responsive galactinol synthase gene from Medicago falcata (MfGolS1) is induced by myo-inositol and confers multiple tolerances to abiotic stresses. Physiol. Plant. 149, 67-78.