The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants

Free Radical Biology and Medicine

Volumn 56, Issue , 2013, Pages 172-183

  Filippou, Panagiota ^a   Antoniou, Chrystalla ^a   Fotopoulos, Vasileios ^a  

^a CYPRUS UNIVERSITY OF TECHNOLOGY   (Cyprus)

Author keywords

Free radicals; Medicago; Nitrosative stress; Polyamines; Proline; Sodium nitroprusside

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; AMINE OXIDASE (COPPER CONTAINING); ARGININE DECARBOXYLASE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; POLYAMINE; POLYAMINE OXIDASE; PROLINE; PYRROLINE 5 CARBOXYLATE REDUCTASE; SPERMIDINE SYNTHASE; SPERMINE SYNTHASE;

ARTICLE; BARREL MEDIC; BIOSYNTHESIS; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; METABOLISM; NONHUMAN; PHOTOSYNTHETIC RATE; PLANT DEVELOPMENT; PLANT LEAF; PRIORITY JOURNAL; STOMATAL CONDUCTANCE;

DOSE-RESPONSE RELATIONSHIP, DRUG; MEDICAGO TRUNCATULA; NITRIC OXIDE DONORS; NITROPRUSSIDE; PLANT LEAVES; POLYAMINES; PROLINE; STRUCTURE-ACTIVITY RELATIONSHIP;

MEDICAGO; MEDICAGO TRUNCATULA;

EID: 84874118202     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.09.037     Document Type: Article

References (87)

1. S.J. Neill, R. Desikan, and J.T. Hancock Nitric oxide signaling in plants New Phytol. 159 2003 11 35
2. C.G. Mata, and L. Lamattina Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress Plant Physiol 126 2001 1196 1204
3. Y.Y. Leshem, E. Haramaty, D. Iluz, Z. Malik, Y. Sofer, L. Roitman, and Y. Leshem Effect of stress nitric oxide (NO): interaction between chlorophyll fluorescence, galactolipid fluidity and lipoxygenase activity Plant Physiol. Biochem. 35 1997 573 579
4. M.V. Beligni, and L. Lamattina Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues Planta 208 1999 337 344
5. Y.T. Hsu, and C.H. Kao Cadmium toxicity is reduced by nitric oxide in rice leaves Plant Growth Regul. 42 2004 227 238
6. N.V. Laspina, M.D. Groppa, M.L. Tomaro, and M.P. Benavides Nitric oxide protects sunflower leaves against Cd-induced oxidative stress Plant Sci. 169 2005 323 330
7. M.V. Beligni, and L. Lamattina Nitric oxide: a non-traditional regulator of plant growth Trends Plant Sci. 6 2001 508 509
8. M.C. Romero-Puertas, M. Perazzolli, E.D. Zago, and M. Delledonne Nitric oxide signalling functions in plant-pathogen interactions Cell. Microbiol. 6 2004 795 803
9. A. Molassiotis, and V. Fotopoulos Oxidative and nitrosative signaling in plants: two branches in the same tree? Plant Signaling Behav 6 2011 210 214
10. A. Schutzendubel, and A. Polle Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization J. Exp. Bot. 53 2002 1351 1365
11. A. Bouchereau, A. Aziz, F. Larher, and J. Martin-Tanguy Polyamines and environmental challenges: recent development Plant Sci. 140 1999 103 125
12. A. Kuthanová, L. Gemperlová, S. Zelenková, J. Eder, I. Machácková, Z. Opatrny, and M. Cvikrová Cytological changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells Plant Physiol. Biochem. 42 2004 149 156
13. X. Xu, G. Shi, C. Ding, Y. Xu, J. Zhao, H. Yang, and Q. Pan Regulation of exogenous spermidine on the reactive oxygen species level and polyamine metabolism in Alternanthera philoxeroides (Mart.) Griseb under copper stress Plant Growth Regul. 63 2011 251 258
14. J. Floryszak-Wieczorek, G. Milczarek, M. Arasimowicz, and A. Ciszewski Do nitric oxide donors mimic endogenous NO-related response in plants? Planta 224 2006 1363 1372
15. L. Ederli, L. Reale, L. Madeo, F. Ferranti, C. Gehring, M. Fornaciari, B. Romano, and S. Pasqualini NO release by nitric oxide donors in vitro and in planta Plant Physiol. Biochem. 47 2009 42 48
16. +-ATPase activation Planta 231 2010 1025 1036
17. R. Kaur-Sawhney, A.F. Tiburcio, T. Altabella, and A.W. Galston Polyamines in plants: an overview J. Cell Mol. Biol. 2 2003 1 12
18. C. Hanfrey, S. Sommer, M.J. Mayer, D. Burtin, and A.J. Michael Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity Plant J. 27 2001 551 560
19. R. Alcázar, T. Altabella, F. Marco, C. Bortolotti, M. Reymond, C. Koncz, P. Carrasco, and A.F. Tiburcio Polyamines: molecules with regulatory functions in plant abiotic stress tolerance Planta 231 2010 1237 1249
20. M. Goyal, and B. Asthir Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress Plant Growth Regul 60 2010 13 25
21. M.D. Groppa, and M.P. Benavides Polyamines and abiotic stress: recent advances Amino Acids 34 2008 35 45
22. P.B. Kavi Kishor, S. Sangam, R.N. Amrutha, P. Sri Laxmi, K.R. Naidu, K.R.S.S. Rao, S. Rao, K.J. Reddy, P. Theriappan, and N. Sreenivasulu Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance Curr. Sci. 88 2005 424 438
23. M. Ashraf, and M.R. Foolad Roles of glycinebetaine and proline in improving plant abiotic stress tolerance Environ. Exp. Bot. 59 2007 206 216
24. I. Yazici, I. Turkan, A.H. Sekmen, and T. Demiral Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation Environ. Exp. Bot. 61 2007 49 57
25. S.S. Sharma, and K.J. Dietz The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress J. Exp. Bot 57 2006 711 726
26. H.J. Gao, H.Q. Yang, and J.X. Wang Arginine metabolism in roots and leaves of apple (Malus domestica Borkh.): the tissue-specific formation of both nitric oxide and polyamines Sci. Hortic 119 2009 147 152
27. N.N. Tun, C. Santa-Catarina, T. Begum, V. Silveira, W. Handro, E.I.S. Floh, and G.F.E. Scherer Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings Plant Cell Physiol. 47 2006 346 354
28. H.E. Flores, and A.W. Galston Analysis of polyamines in higher plants by high performance liquid chromatography Plant Physiol. 69 1982 701 706
29. K. Kotzabasis, M.D. Hampsas-Christakis, and K.A. Angelakis-Roubelakis A narrow-bore HPLC method for the identification and quantitation of free, conjugated and bound polyamines Anal. Biochem. 214 1993 484 489
30. L.S. Bates, R.P. Waldren, and E.D. Teare Rapid determination of free proline for stress studies Plant Soil. 39 1973 205 208
31. P. Filippou, C. Antoniou, and V. Fotopoulos Effect of drought and rewatering on the antioxidant response of Medicago truncatula plants Plant Signaling Behav 6 2011 270 277
32. W.-G. Wang, R. Li, B. Liu, L. Li, S.-H. Wang, and F. Chen Effects of low nitrogen and drought stresses on proline synthesis of Jatropha curcas seedling Acta Physiol. Plant. 33 2011 1591 1595
33. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem 72 1976 248 254
34. A.E. Koromilas, and D.A. Kyriakidis Purification and properties of ornithine decarboxylase from germinated barley seeds Phytochemistry 27 1988 989 992
35. 2 production in the chalazal cells during barley grain filling J. Exp. Bot. 53 2002 677 682
36. M. Quinet, A. Ndayiragije, I. Lefevre, B. Lambillotte, C.C. Dupont-Gillain, and S. Lutts Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance J. Exp. Bot. 61 2010 2719 2733
37. H. Mhadhbi, V. Fotopoulos, P.V. Mylona, M. Jebara, M.E. Aouani, and A.N. Polidoros Role of antioxidant gene-enzyme responses in Medicago truncatula genotypes with different degrees of sensitivity to high salinity Physiol. Plant. 141 2011 201 214
38. M.W. Pfaffl, G.W. Horgan, and L. Dempfle Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR Nucleic Acids Res 30 2002 e36 2002
39. L. Lamattina, C. Garcia-Mata, M. Graziano, and G. Pagnussat Nitric oxide: the versatility of an extensive signal molecule Annu. Rev. Plant Biol. 54 2003 109 136
40. J.G. Filep, C. Lapierre, S. Lachance, and J.S.D. Chan Nitric oxide co-operates with hydrogen peroxide in inducing DNA fragmentation and cell lysis in murine lymphoma cells Biochem. J. 321 1997 897 901
41. J.J. Duan, J. Li, S.R. Guo, and Y.Y. Kang Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance J. Plant Physiol. 165 2008 1620 1635
42. V. Velikova, I. Yordanov, and A. Edreva Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines Plant Sci 151 2000 59 66
43. R. Wimalasekera, and G.F.E. Scherer Polyamines and cytokinin: is nitric oxide biosynthesis the key to overlapping functions? S. Hayat, M. Mori, J. Pichtel, A. Ahmad, Nitric Oxide in Plant Physiology 2010 Wiley VCH Weinheim 65 76
44. K. Urano, K. Maruyama, Y. Ogata, Y. Morishita, M. Takeda, N. Sakurai, H. Suzuki, K. Saito, D. Shibata, M. Kobayashi, K. Yamaguchi-Shinozaki, and K. Shinozaki Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics Plant J. 57 2009 1065 1078
45. M.D. Groppa, E.P. Rosales, M.F. Iannone, and M.P. Benavides Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots Phytochemistry 69 2008 2609 2615
46. P. Filippou, C. Antoniou, S. Yelamanchili, and V. Fotopoulos NO loading: efficiency assessment of five commonly used application methods of sodium nitroprusside in Medicago truncatula plants Plant Physiol. Biochem. 60 2012 115 118
47. C. Masgrau, T. Altabella, R. Farrás, D. Flores, A.J. Thompson, R.T. Besford, and A.F. Tiburcio Inducible overexpression of oat arginine decarboxylase in transgenic tobacco plants Plant J. 11 1997 465 473
48. T. Koichi, M. Rickhag, C. Hegardt, S. Oredsson, and L. Persson Induction of apoptotic cell death by putrescine Int. J. Biochem. Cell Biol. 38 2006 621 628
49. J.C. Cuevas, R. Lopez-Cobollo, R. Alcázar, X. Zarza, C. Koncz, T. Altabella, J. Salinas, A.F. Tiburcio, and A. Ferrando Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature Plant Physiol. 148 2008 1094 1105
50. R. Alcázar, J.C. Cuevas, J. Planas, X. Zarza, C. Bortolotti, P. Carrasco, J. Salinas, A.F. Tiburcio, and T. Altabella Integration of polyamines in the cold acclimation response Plant Sci. 180 2011 31 38
51. X. Xu, G. Shi, and R. Jia Changes of polyamine levels in roots of Sagittaria sagittifolia L. under copper stress Environ. Sci. Pollut. Res. 19 2012 2973 2982
52. S.S. Verma, and N. Mishra Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system J. Plant Physiol 162 2005 669 677
53. A. Ndayiragije, and S. Lutts Long term exogenous putrescine application improves grain yield of a salt-sensitive rice cultivar exposed to NaCl Plant Soil 29 2007 225 238
54. Fan, H.-F.; Du, C.-X.; Guo, S.-R. Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. Environ. Exp. Bot. 10.1016/j.envexpbot.2010.09.007, in press
55. W. Zhang, B. Jiang, W. Li, H. Song, Y. Yu, and J. Chen Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system Sci. Hortic 122 2009 200 208
56. M.A. Perez-Amador, J. Leon, P.J. Green, and J. Carbonell Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis Plant Physiol 130 2002 1454 1463
57. S.S. Hussain, M. Ali, M. Ahmad, and K.H.M. Siddique Polyamines: natural and engineered abiotic and biotic stress tolerance in plants Biotechnol. Adv. 29 2011 300 311
58. I. Couee, I. Hummel, C. Sulmon, G. Gouesbet, and A.E. Amrani Involvement of polyamines in root development Plant Cell Tissue Organ Cult. 76 2004 1 10
59. J. Shi, X.Z. Fu, T. Peng, X.S. Huang, Q.J. Fan, and J.H. Liu Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response Tree Physiol. 30 2010 914 922
60. J. Yang, J. Zhang, K. Liu, Z. Wang, and L. Liu Involvement of polyamines in the drought resistance of rice J. Exp. Bot. 58 2007 1545 1555
61. R. Alcázar, J. Planas, T. Saxena, X. Zarza, C. Bortolotti, J. Cuevas, M. Bitrián, A.F. Tiburcio, and T. Altabella Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous arginine decarboxylase 2gene Plant Physiol. Biochem. 48 2010 547 552
62. A.I. Alet, D.H. Sanchez, J.C. Cuevas, S. del Valle, T. Altabella, A.F. Tiburcio, F. Marco, A. Ferrando, F.D. Espasandνn, M.E. Gonzalez, P. Carrasco, and O.A. Ruiz Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress Plant Signaling Behav 6 2011 278 286
63. A. Tassoni, S. Fornale, and N. Bagni Putative ornithine decarboxylase activity in Arabidopsis thaliana: inhibition and intracellular localization Plant Physiol. Biochem. 41 2003 871 877
64. J. Legocka, and A. Kluk Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinus luteus seedlings J. Plant Physiol 162 2005 662 668
65. Q.-S. Wu, X.-H. He, Y.-N. Zou, C.-Y. Liu, J. Xiao, and Y. Li Arbuscular mycorrhizas alter root system architecture of citrus tangerine through regulating metabolism of endogenous polyamines Plant Growth Regul 68 2012 27 35
66. 2 signatures that direct tolerance responses in tobacco Plant Cell 20 2008 1708 1724
67. H. Fan, S. Guo, Y. Jiao, R. Zhang, and J. Li Effects of exogenous nitric oxide on growth, active oxygen species metabolism and photosynthetic characteristics in cucumber seedlings under NaCl stress Front. Agric. China 1 2007 308 314
68. C. Delis, M. Dimou, E. Flemetakis, G. Aivalakis, and P.A. Katinakis Root- and hypocotyl-specific gene coding for copper-containing amine oxidase is related to cell expansion in soybean seedlings J. Exp. Bot. 57 2006 101 111
69. R. Wimalasekera, F. Tebartz, and G.F. Scherer Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses Plant Sci. 181 2011 593 603
70. A. Cona, G. Rea, R. Angelini, R. Federico, and P. Tavladoraki Functions of amine oxidases in plant development and defence Trends Plant Sci. 11 2006 80 88
71. H. Liu, R. Colavitti, I.I. Rovira, and T. Finkel Redox-dependent transcriptional regulation Circ. Res. 97 2005 967 974
72. 2 mediating tolerance of plants to abiotic stress: a synergistic signalling approach J. Stress Physiol. Biochem 7 2011 34 74
73. A. Borrell, R.T. Besford, T. Altabella, C. Masgrau, and A.F. Tiburcio Regulation of arginine decarboxylase by spermine in osmotically-stressed oat leaves Physiol. Plant 98 1996 105 110
74. P. Thu-Hang, L. Bassie, G. Safwat, P. Trung-Nghia, P. Christou, and T. Capell Expression of a heterologous S-adenosylmethionine decarboxylase cDNA in plants demonstrates that changes in S-adenosyl-l-methionine decarboxylase activity determine levels of the higher polyamines spermidine and spermine Plant Physiol 129 2002 1744 1754
75. W.-W. Hu, H. Gong, and E.-C. Pua Molecular cloning and characterization of S-adenosylmethionine decarboxylase genes from mustard (Brassica juncea) Plant Physiol 124 2005 25 40
76. X. Hu, Y. Zhang, Y. Shi, Z. Zhang, Z. Zou, H. Zhang, and J. Zhao Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress Plant Physiol. Biochem. 57 2012 200 209
77. C. Vergnolle, M.N. Vaultier, L. Taconnat, J.P. Renou, J.C. Kader, A. Zachowski, and E. Ruelland The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions Plant Physiol. 139 2005 1217 1233
78. K. Takao, M. Rickhag, C. Hegardt, S. Oredsson, and L. Persson Induction of apoptotic cell death by putrescine Int. J. Biochem. Cell Biol. 38 2006 621 628
79. S.S. Gill, and N. Tuteja Polyamines and abiotic stress tolerance in plants Plant Signaling Behav 5 2010 26 33
80. S. Mohapatra, R. Minocha, S. Long, and S.C. Minocha Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids Amino Acids 38 2010 1117 1129
81. L.P. Zhang, S.K. Mehta, Z.P. Liu, and Z.M. Yang Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii Plant Cell Physiol. 49 2008 411 419
82. L. Szabados, and A. Savouré Proline: a multifunctional amino acid Trends Plant Sci. 15 2009 89 97
83. S. Sharma, and P.E. Verslues Mechanisms independent of ABA or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery Plant Cell Environ 33 2010 1838 1851
84. J.A. de Ronde, W.A. Cress, G.H.J. Kruger, R.J. Strasser, and J. Van Staden Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress J. Plant Physiol. 161 2004 1211 1224
85. P.D. Hare, W.A. Cress, and J. Van Staden Dissecting the roles of osmolyte accumulation during stress Plant Cell Environ. 21 1998 535 553
86. A. Phutela, V. Jain, K. Dhawan, and H.S. Nainawatee Proline metabolism under water stress in the leaves and roots of Brassica juncea cultivars differing in drought tolerance J. Plant Biochem. Biotechnol. 9 2000 35 39
87. R. Mattioli, P. Costantino, and M. Trovato Proline accumulation in plants: not only stress Plant Signaling Behav 4 2009 1016 1018