Sodic alkaline stress mitigation by interaction of nitric oxide and polyamines involves antioxidants and physiological strategies in Solanum lycopersicum

Free Radical Biology and Medicine

Volumn 71, Issue , 2014, Pages 36-48

  Gong, Biao ^a   Li, Xiu ^a   Bloszies, Sean ^b   Wen, Dan ^a   Sun, Shasha ^a   Wei, Min ^a   Li, Yan ^a   Yang, Fengjuan ^a   Shi, Qinghua ^a   Wang, Xiufeng ^a  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Alkaline stress; Alleviating effects; Free radicals; Nitric oxide; Oxidative stress; Polyamines; Tomato

Indexed keywords

ADENOSYLMETHIONINE DECARBOXYLASE; ANTIOXIDANT; ARGININE DECARBOXYLASE; ASCORBATE PEROXIDASE; CALCIUM ION; CATALASE; DEHYDROASCORBIC ACID REDUCTASE; GLUTATHIONE REDUCTASE; GUAIACOL PEROXIDASE; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGUAZONE; NITRIC OXIDE; POLYAMINE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SODIUM PROTON EXCHANGE PROTEIN; SPERMIDINE SYNTHASE; SPERMINE SYNTHASE; SUPEROXIDE DISMUTASE; 1,3-DIHYDROXY-4,4,5,5-TETRAMETHYL-2-(4-CARBOXYPHENYL)TETRAHYDROIMIDAZOLE; BENZOIC ACID DERIVATIVE; CALCIUM; IMIDAZOLE DERIVATIVE; SODIUM HYDROXIDE;

ABIOTIC STRESS; ARTICLE; CHLOROPHYLL CONTENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; PLANT GROWTH; PLANT LEAF; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SODIUM TRANSPORT; STRESS; TOMATO; WATER CONTENT; ADAPTATION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HYDROPONICS; METABOLISM; PHYSIOLOGICAL STRESS; PLANT ROOT; SEEDLING; TRANSPORT AT THE CELLULAR LEVEL;

ADAPTATION, PHYSIOLOGICAL; ANTIOXIDANTS; BENZOATES; BIOLOGICAL TRANSPORT; CALCIUM; GENE EXPRESSION REGULATION, PLANT; HYDROPONICS; IMIDAZOLES; LYCOPERSICON ESCULENTUM; MITOGEN-ACTIVATED PROTEIN KINASES; MITOGUAZONE; NITRIC OXIDE; PLANT ROOTS; POLYAMINES; REACTIVE OXYGEN SPECIES; SEEDLING; SIGNAL TRANSDUCTION; SODIUM HYDROXIDE; SODIUM-HYDROGEN ANTIPORTER; STRESS, PHYSIOLOGICAL;

EID: 84898767359     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.02.018     Document Type: Article

References (46)

1. B. Gong, D. Wen, K. VandenLangenberg, M. Wei, F. Yang, Q. Shi, and X. Wang Comparative effects of NaCl and NaHCO3 stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves Sci. Hortic. 157 2013 1 12
2. Z.H. Ren, J.P. Gao, L.G. Li, X.L. Cai, W. Huang, D.Y. Chao, M.Z. Zhu, Z.Y. Wang, S. Luan, and H.X. Lin A rice quantitative trait locus for salt tolerance encodes a sodium transporter Nat. Genet. 37 2005 1141 1146 (Pubitemid 41486670)
3. W. Xu, L. Jia, F. Baluška, G. Ding, W. Shi, N. Ye, and J. Zhang PIN2 is required for the adaptation of Arabidopsis roots to alkaline stress by modulating proton secretion J. Exp. Bot. 63 2012 6105 6114
4. S.J. Neill, R. Desikan, and J.T. Hancock Nitric oxide signaling in plants New Phytol. 159 2003 11 35
5. A. Besson-Bard, A. Pugin, and D. Wendehenne New insights into nitric oxide signaling in plants Annu. Rev. Plant Biol. 59 2008 21 39 (Pubitemid 351813022)
6. M. Arasimowicz, and J. Floryszak-Wieczorek Nitric oxide as a bioactive signalling molecule in plant stress responses Plant Sci. 172 2007 876 887 (Pubitemid 46517737)
7. S. Neill, R. Barros, J. Bright, R. Desikan, J. Hancock, J. Harrison, P. Morris, D. Ribeiro, and L. Wilson Nitric oxide, stomatal closure, and abiotic stress J. Exp. Bot. 59 2008 165 176 (Pubitemid 351651356)
8. M. Leterrier, M. Chaki, M. Airaki, R. Valderrama, J.M. Palma, J.B. Barroso, and F.J. Corpas Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress Plant Signaling Behav. 6 2011 789 793
9. 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
10. S.S. Gill, and N. Tuteja Polyamines and abiotic stress tolerance in plants Plant Signaling Behav. 5 2010 26 33
11. S.S. Hussain, M. Ali, M. Ahmad, and K.H. Siddique Polyamines: natural and engineered abiotic and biotic stress tolerance in plants Biotechnol. Adv. 29 2011 300 311
12. 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 (Pubitemid 43238419)
13. 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
14. S. Shu, S.R. Guo, J. Sun, and L.Y. Yuan Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine Physiol. Plant. 146 2012 285 296
15. S. Shu, L.Y. Yuan, S.R. Guo, J. Sun, and Y.H. Yuan Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress Plant Physiol. Biochem. 63 2013 209 216
16. M. Arasimowicz-Jelonek, J. Floryszak-Wieczorek, and J. Kubis Interaction between polyamine and nitric oxide signaling in adaptive responses to drought in cucumber J. Plant Growth Regul. 28 2009 177 186
17. H. Yamasaki, and M.F. Cohen NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci. 11 2006 522 524 (Pubitemid 44636301)
18. N.N. Tun, A. Holk, and G.F.E. Scherer Rapid increase of NO release in plant cell cultures induced by cytokinin FEBS Lett. 509 2001 174 176 (Pubitemid 34015937)
19. 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
20. P. Filippou, C. Antoniou, and V. Fotopoulos The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants Free Radic. Biol. Med. 56 2013 172 183
21. D.R. Hoagland, and D.I. Arnon The Water-Culture Method for Growing Plants without Soil. California Agricultural Experiment Station Circular 347 1938 Univ. of California Berkeley
22. K. Maxwell, and G.N. Johnson Chlorophyll fluorescence - a practical guide J. Exp. Bot. 51 2000 659 668 (Pubitemid 30254655)
23. F. Liu, and F.Q. Guo Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis PLoS One 8 2013 1 12
24. H. Zhang, Z. Huang, B. Xie, Q. Chen, X. Tian, X. Zhang, H. Zhang, X. Lu, D. Huang, and R. Huang The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco Planta 220 2004 262 270 (Pubitemid 40084184)
25. X.J. Xia, Y.J. Wang, Y.H. Zhou, Y. Tao, W.H. Mao, K. Shi, T. Asami, Z. Chen, and J.Q. Yu Reactive oxygen species are involved in brassinosteroid- induced stress tolerance in cucumber Plant Physiol. 150 2009 801 814
26. C. Capone, M. Cervelli, E. Angelucci, M. Colasanti, A. Macone, P. Mariottini, and T. Persichini A role for spermine oxidase as a mediator of reactive oxygen species production in HIV-Tat-induced neuronal toxicity Free Radic. Biol. Med. 63 2013 99 107
27. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29 2001 e45
28. M. Moreau, G.I. Lee, Y. Wang, B.R. Crane, and D.F. Klessig AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase J. Biol. Chem. 283 2008 32957 32967
29. M. Airaki, M. Leterrier, R.M. Mateos, R. Valderrama, M. Chaki, J.B. Barroso, L.A. del Río, J.M. Palma, and F.J. Corpas Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress Plant Cell Environ. 35 2011 281 295
30. M. Chaki, R. Valderrama, A.M. Fernández-Ocaña, A. Carreras, M.V. Gómez-Rodríguez, J.R. Pedrajas, J.C. Begara-Morales, B. Sánchez-Calvo, F. Luque, M. Leterrier, F.J. Corpas, and J.B. Barroso Mechanical wounding induces a nitrosative stress by downregulation of GSNO reductase and a rise of S-nitrosothiols in sunflower (Helianthus annuus) seedlings J. Exp. Bot. 62 2011 1803 1813
31. 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
32. R. Olías, Z. Eljakaoui, J. Li, P.A.D. Morales, M.C. Marín-Manzano, J.M. Pardo, and A. Belver The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs Plant Cell Environ. 32 2009 904 916
33. E. Blumwald, G.S. Aharon, and M.P. Apse Sodium transport in plant cells Biochim. Biophys. Acta 1465 2000 140 151 (Pubitemid 30169065)
34. Y. Zhang, L. Wang, Y. Liu, Q. Zhang, Q. Wei, and W. Zhang Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast Planta 224 2006 545 555 (Pubitemid 44188099)
35. S. Fukada-Tanaka, Y. Inagaki, T. Yamaguchi, N. Saito, and S. Iida Colour-enhancing protein in blue petals Nature 407 2000 581
36. J.S. Chung, J.K. Zhu, R.A. Bressan, P.M. Hasegawa, and H.Z. Shi Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis Plant J. 53 2008 554 565 (Pubitemid 351172025)
37. M.P. Zhang, C.J. Zhang, G.H. Yu, Y.Z. Jiang, R.J. Strasser, Z.Y. Yuan, X.S. Yang, and G.X. Chen Changes in chloroplast ultrastructure, fatty acid components of thylakoid membrane and chlorophyll a fluorescence transient in flag leaves of a super-high-yield hybrid rice and its parents during the reproductive stage J. Plant Physiol. 167 2010 277 285
38. P. Jaspers, and J. Kangasjärvi Reactive oxygen species in abiotic stress signaling Physiol. Plant. 138 2010 405 413
39. R.T. Besford, C.M. Richardson, J.L. Campos, and A.F. Tiburcio Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves Planta 189 1993 201 206
40. J.F. Poduslo, and G.L. Curran Increased permeability of superoxide dismutase at the blood-nerve and blood-brain barriers with retained enzymatic activity after covalent modification with the naturally occurring polyamine, putrescine J. Neurochem. 67 1996 734 741 (Pubitemid 26255671)
41. N. Suzuki, S. Koussevitzky, R. Mittler, and G. Miller ROS and redox signalling in the response of plants to abiotic stress Plant Cell Environ. 35 2012 259 270
42. R.K. Tewari, S. Kim, E.J. Hahn, and K.Y. Paek Involvement of nitric oxide-induced NADPH oxidase in adventitious root growth and antioxidant defense in Panax ginseng Plant Biotechnol. Rep. 2 2008 113 122 (Pubitemid 351814526)
43. D. Clark, J. Durner, D.A. Navarre, and D.F. Klessig Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase Mol. Plant-Microbe Interact. 13 2000 1380 1384
44. S. Orellana, M. Yañez, A. Espinoza, I. Verdugo, E. González, S. Ruiz-Lara, and J.A. Casaretto The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato Plant Cell Environ. 33 2010 2191 2280
45. Y. Pan, G.B. Seymour, C. Lu, Z. Hu, X. Chen, and G. Chen An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato Plant Cell Rep. 31 2012 349 360
46. S. D'Alessandro, B. Posocco, A. Costa, G. Zahariou, F.L. Schiavo, D. Carbonera, and M. Zottini Limits in the use of cPTIO as nitric oxide scavenger and EPR probe in plant cells and seedlings Front. Plant Sci. 4 2013 1 7