Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: A comparison with responses to drought

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Do, Phuc T ^a,c   Drechsel, Oliver ^a,d   Heyer, Arnd G ^b   Hincha, Dirk K ^a   Zuther, Ellen ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIVERSITY OF STUTTGART   (Germany)

^c VIETNAM NATIONAL UNIVERSITY   (Viet Nam)

^d CENTRE FOR GENOMIC REGULATION CRG   (Spain)

Author keywords

Drought stress; Gene expression; Natural variety; Polyamines; Rice; Salt stress

Indexed keywords

EID: 84901029113     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00182     Document Type: Article

References (108)

1. Acosta, C., Perez-Amador, M. A., Carbonell, J., and Granell, A. (2005). The two ways to produce putrescine in tomato are cell-specific during normal development. Plant Sci. 168, 1053-1057. doi: 10.1016/j.plantsci.2004.12.006
2. Akita, S., and Cabuslay, G. (1990). "Physiological basis of differential response to salinity in rice cultivars, " in Genetic Aspects of Plant Mineral Nutrition, eds N. Bassam, M. Dambroth, and B. C. Loughman (Netherlands: Springer), 431-448.
3. Alcázar, R., Bitrian, M., Bartels, D., Koncz, C., Altabella, T., and Tiburcio, A. F. (2011). Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signal. Behav. 6, 243-250. doi: 10.4161/psb.6.2.14317
4. Alcázar, R., Cuevas, J. C., Patron, M., Altabella, T., and Tiburcio, A. F. (2006b). Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol. Plant. 128, 448-455. doi: 10.1111/j.1399-3054.2006.00780.x
5. Alcázar, R., Marco, F., Cuevas, J., Patron, M., Ferrando, A., Carrasco, P., et al. (2006a). Involvement of polyamines in plant response to abiotic stress. Biotechnol. Lett. 28, 1867-1876. doi: 10.1007/s10529-006-9179-3
6. Alcázar, R., Planas, J., Saxena, T., Zarza, X., Bortolotti, C., Cuevas, J., et al. (2010). Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous arginine decarboxylase 2 gene. Plant Physiol. Biochem. 48, 547-552. doi: 10.1016/j.plaphy.2010.02.002
7. Alet, A. I., Sanchez, D. H., Cuevas, J. C., Del Valle, S., Altabella, T., Tiburcio, A. F., et al. (2011a). Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal. Behav. 6, 78-286. doi: 10.4161/psb.6.2.14702
8. Alet, A. I., Sánchez, D. H., Cuevas, J. C., Marina, M., Carrasco, P., Altabella, T., et al. (2012). New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci. 182, 94-100. doi: 10.1016/j.plantsci.2011.03.013
9. Alet, A. I., Sanchez, D. H., Ferrando, A., Tiburcio, A. F., Alcazar, R., Cuevas, J. C., et al. (2011b). Homeostatic control of polyamine levels under long-term salt stress in Arabidopsis. Plant Signal. Behav. 6, 237-242. doi: 10.4161/psb.6.2.14214
10. Aziz, A., and Larher, F. (1995). Changes in polyamine titers associated with the proline response and osmotic adjustment of rape leaf discs submitted to osmotic stresses. Plant Sci. 112, 175-186. doi: 10.1016/0168-9452(95)04264-4
11. Aziz, A., Martin-Tanguy, J., and Larher, F. (1997). Plasticity of polyamine metabolism associated with high osmotic stress in rape leaf discs and with ethylene treatment. Plant Growth Regul. 21, 153-163. doi: 10.1023/A:1005730509433
12. Aziz, A., Martin-Tanguy, J., and Larher, F. (1999). Salt stress-induced proline accumulation and changes in tyramine and polyamine levels are linked to ionic adjustment in tomato leaf discs. Plant Sci. 145, 83-91. doi: 10.1016/S0168-9452(99)00071-0
13. Basu, R., and Ghosh, B. (1991). Polyamines in various rice (Oryza sativa) genotypes with respect to sodium chloride salinity. Physiol. Plant. 82, 575-581. doi: 10.1111/j.1399-3054.1991.tb02949.x
14. Basu, R., Maitra, N., and Ghosh, B. (1988). Salinity results in polyamine accumulation in early rice (Oryza sativa L.). seedlings. Funct. Plant Biol. 15, 777-786.
15. Birecka, H., Bitonti, A. J., and Mccann, P. P. (1985). Assaying ornithine and arginine decarboxylases in some plant species. Plant Physiol. 79, 509-514. doi: 10.1104/pp.79.2.509
16. Bitrián, M., Zarza, X., Altabella, T., Tiburcio, A. F., and Alcázar, R. (2012). Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites 2, 516-528. doi: 10.3390/metabo2030516
17. Borrell, A., Culianez-Macia, F. A., Altabella, T., Besford, R. T., Flores, D., and Tiburcio, A. F. (1995). Arginine decarboxylase is localized in chloroplasts. Plant Physiol. 109, 771-776. doi: 10.1104/pp.109.3.771
18. Bouchereau, A., Aziz, A., Larher, F., and Martin-Tanguy, J. (1999). Polyamines and environmental challenges: recent development. Plant Sci. 140, 103-125. doi: 10.1016/S0168-9452(98)00218-0
19. 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. U.S.A. 101, 9909-9914. doi: 10.1073/pnas.0306974101
20. Capell, T., Escobar, C., Liu, H., Burtin, D., Lepri, O., and Christou, P. (1998). Over-expression of the oat arginine decarboxylase cDNA in transgenic rice (Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theor. Appl. Genet. 97, 246-254. doi: 10.1007/s001220050892
21. Chattopadhyay, M. K., Gupta, S., Sengupta, D. N., and Ghosh, B. (1997). Expression of arginine decarboxylase in seedlings of indica rice (Oryza sativa L.) cultivars as affected by salinity stress. Plant Mol. Biol. 34, 477-493. doi: 10.1023/A:1005802320672
22. Chattopadhyay, M. K., Tiwari, B. S., Chattopadhyay, G., Bose, A., Sengupta, D. N., and Ghosh, B. (2002). Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol. Plant. 116, 192-199. doi: 10.1034/j.1399-3054.2002.1160208.x
23. Cha-Um, S., Supaibulwatana, K., and Kirdmanee, C. (2006). Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativa L. ssp. indica cv. KDML 105) to salt stress by application of exogenous glycinebetaine and choline. J. Agron. Crop Sci. 192, 25-36. doi: 10.1111/j.1439-037X.2006.00186.x
24. Chinnusamy, V., Jagendorf, A., and Zhu, J.-K. (2005). Understanding and improving salt tolerance in plants. Crop Sci. 45, 437-448. doi: 10.2135/cropsci2005.0437
25. Cohen, S. (1998). A Guide to the Polyamines. New York, NY: Oxford University Press.
26. Degenkolbe, T., Do, P. T., Kopka, J., Zuther, E., Hincha, D. K., and Köhl, K. I. (2013). Identification of drought tolerance markers in a diverse population of rice cultivars by expression and metabolite profiling. PLoS ONE 8:e63637. doi: 10.1371/journal.pone.0063637
27. Degenkolbe, T., Do, P., Zuther, E., Repsilber, D., Walther, D., Hincha, D., et al. (2009). Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Mol. Biol. 69, 133-153. doi: 10.1007/s11103-008-9412-7
28. Dionisio-Sese, M. L., and Tobita, S. (2000). Effects of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. J. Plant Physiol. 157, 54-58. doi: 10.1016/S0176-1617(00)80135-2
29. Do, P. T., Degenkolbe, T., Erban, A., Heyer, A. G., Kopka, J., Köhl, K. I., et al. (2013). Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS ONE 8:e60325. doi: 10.1371/journal.pone.0060325
30. Flores, H. E., and Galston, A. W. (1982). Polyamines and plant stress: activation of putrescine biosynthesis by osmotic shock. Science 217, 1259-1261. doi: 10.1126/science.217.4566.1259
31. Galston, A. W., and Sawhney, R. K. (1990). Polyamines in plant physiology. Plant Physiol. 94, 406-410. doi: 10.1104/pp.94.2.406
32. Gill, S. S., and Tuteja, N. (2010). Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 5, 26-33. doi: 10.4161/psb.5.1.10291
33. Gupta, K., Dey, A., and Gupta, B. (2013). Plant polyamines in abiotic stress responses. Acta Physiol. Plant. 35, 2015-2036. doi: 10.1007/s11738-013-1239-4
34. Hao, Y.-J., Kitashiba, H., Honda, C., Nada, K., and Moriguchi, T. (2005a). Expression of arginine decarboxylase and ornithine decarboxylase genes in apple cells and stressed shoots. J. Exp. Bot. 56, 1105-1115. doi: 10.1093/jxb/eri102
35. Hao, Y.-J., Zhang, Z., Kitashiba, H., Honda, C., Ubi, B., Kita, M., et al. (2005b). Molecular cloning and functional characterization of two apple S-adenosylmethionine decarboxylase genes and their different expression in fruit development, cell growth and stress responses. Gene 350, 41-50. doi: 10.1016/j.gene.2005.01.004
36. Hultgren, A., and Rau, D. C. (2004). Exclusion of alcohols from spermidine-DNA assemblies: probing the physical basis of preferential hydration. Biochemistry 43, 8272-8280. doi: 10.1021/bi049559s
37. Hussain, S. S., Ali, M., Ahmad, M., and Siddique, K. H. M. (2011). Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol. Adv. 29, 300-311. doi: 10.1016/j.biotechadv.2011.01.003
38. Kakkar, R. K., and Sawhney, V. K. (2002). Polyamine research in plants-a changing perspective. Physiol. Plant. 116, 281-292. doi: 10.1034/j.1399-3054.2002.1160302.x
39. Karan, R., Deleon, T., Biradar, H., and Subudhi, P. K. (2012). Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS ONE 7:e40203. doi: 10.1371/journal.pone.0040203
40. Kasukabe, Y., He, L., Nada, K., Misawa, S., Ihara, I., and Tachibana, S. (2004). Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol. 45, 712-722. doi: 10.1093/pcp/pch083
41. Katiyar, S., and Dubey, R. S. (1990). Changes in polyamine titer in rice seedlings following NaCl salinity stress. J. Agron. Crop Sci. 165, 19-27. doi: 10.1111/j.1439-037X.1990.tb00830.x
42. Kaur-Sawhney, R., Tiburcio, A. F., Altabella, T., and Galston, A. W. (2003). Polyamines in plants: an overview. J. Cell Mol. Biol. 2, 1-12.
43. Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., et al. (2001). Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13, 889-906. doi: 10.1105/tpc.13.4.889
44. Krishnamurthy, R., and Bhagwat, K. A. (1989). Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol. 91, 500-504. doi: 10.1104/pp.91.2.500
45. Kwak, S.-H., and Lee, S. H. (2001). The regulation of ornithine decarboxylase gene expression by sucrose and small upstream open reading frame in tomato (Lycopersicon esculentum Mill). Plant Cell Physiol. 42, 314-323. doi: 10.1093/pcp/pce040
46. Lahiri, K., Chattopadhyay, S., and Ghosh, B. (2004). Correlation of endogenous free polyamine levels with root nodule senescence in different genotypes in Vigna mungo L. J. Plant Physiol. 161, 563-571. doi: 10.1078/0176-1617-01057
47. Lee, K.-S., Choi, W.-Y., Ko, J.-C., Kim, T.-S., and Gregorio, G. (2003). Salinity tolerance of japonica and indica rice (Oryza sativa L.) at the seedling stage. Planta 216, 1043-1046. doi: 10.1007/s00425-002-0958-3
48. Lefèvre, I., Gratia, E., and Lutts, S. (2001). Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci. 161, 943-952. doi: 10.1016/S0168-9452(01)00485-X
49. Legocka, J., and Kluk, A. (2005). Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinus luteus seedlings. J. Plant Physiol. 162, 662-668. doi: 10.1016/j.jplph.2004.08.009
50. Lester, G. E. (2000). Polyamines and their cellular anti-senescence properties in honey dew muskmelon fruit. Plant Sci. 160, 105-112. doi: 10.1016/S0168-9452(00)00369-1
51. Li, Z.-Y., and Chen, S.-Y. (2000a). Isolation and characterization of a salt-and drought-inducible gene for S-adenosylmethionine decarboxylase from wheat (Triticum aestivum L.). J. Plant Physiol. 156, 386-393. doi: 10.1016/S0176-1617(00)80078-4
52. Li, Z. Y., and Chen, S. Y. (2000b). Differential accumulation of the S-adenosylmethionine decarboxylase transcript in rice seedlings in response to salt and drought stresses. Theor. Appl. Genet. 100, 782-788. doi: 10.1007/s001220051352
53. Lin, C., and Kao, C. (1995). Levels of endogenous polyamines and NaCl-inhibited growth of rice seedlings. Plant Growth Regul. 17, 15-20.
54. Liu, H. P., Dong, B. H., Zhang, Y. Y., Liu, Z. P., and Liu, Y. L. (2004). Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Sci. 166, 1261-1267. doi: 10.1016/j.plantsci.2003.12.039
55. Liu, J.-H., Nada, K., Honda, C., Kitashiba, H., Wen, X.-P., Pang, X.-M., et al. (2006). Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J. Exp. Bot. 57, 2589-2599. doi: 10.1093/jxb/erl018
56. Liu, K., Fu, H., Bei, Q., and Luan, S. (2000). Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol. 124, 1315-1326. doi: 10.1104/pp.124.3.1315
57. Lutts, S., Kinet, J. M., and Bouharmont, J. (1996). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann. Bot. 78, 389-398. doi: 10.1006/anbo.1996.0134
58. Maiale, S., Sanchez, D. H., Guirado, A., Vidal, A., and Ruiz, O. A. (2004). Spermine accumulation under salt stress. J. Plant Physiol. 161, 35-42. doi: 10.1078/0176-1617-01167
59. Marco, F., Alcázar, R., Altabella, T., Carrasco, P., Gill, S. S., Tuteja, N., et al. (2012). "Polyamines in developing stress-resistant crops, " in Improving Crop Resistance to Abiotic Stress eds N. Tuteja, S. S. Gill, A. F. Tiburcio, and R. Tuteja (Weinheim: Wiley-VCH Verlag GmbH & Co. KgaA), 623-635. doi: 10.1002/9783527632930.ch27
60. Marco, F., Alcázar, R., Tiburcio, A. F., and Carrasco, P. (2011). Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS 15, 775-781. doi: 10.1089/omi.2011.0084
61. Martin-Tanguy, J. (2001). Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul. 34, 135-148. doi: 10.1023/A:1013343106574
62. Mattoo, A., Minocha, S., Minocha, R., and Handa, A. (2010). Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38, 405-413. doi: 10.1007/s00726-009-0399-4
63. Mitchell, J. H., Siamhan, D., Wamala, M. H., Risimeri, J. B., Chinyamakobvu, E., Henderson, S. A., et al. (1998). The use of seedling leaf death score for evaluation of drought resistance of rice. Field Crops Res. 55, 129-139. doi: 10.1016/S0378-4290(97)00074-9
64. Mo, H., and Pua, E.-C. (2002). Up-regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. Physiol. Plant. 114, 439-449. doi: 10.1034/j.1399-3054.2002.1140314.x
65. Moschou, P. N., and Roubelakis-Angelakis, K. A. (2013). Polyamines and programmed cell death. J. Exp. Bot. 65, 1285-1296. doi: 10.1093/jxb/ert373
66. 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. doi: 10.1093/jxb/ers202
67. Nakamura, I., Murayama, S., Tobita, S., Bong, B. B., Yanagihara, S., Ishimine, Y., et al. (2002). Effect of NaCl on the photosynthesis, water relations and free proline accumulation in the wild Oryza species. Plant Prod. Sci. 5, 305-310. doi: 10.1626/pps.5.305
68. Ndayiragije, A., and Lutts, S. (2006). Exogenous putrescine reduces sodium and chloride accumulation in NaCl-treated calli of the salt-sensitive rice cultivar I Kong Pao. Plant Growth Regul. 48, 51-63. doi: 10.1007/s10725-005-4825-7
69. Panagiotidis, C. A., Artandi, S., Calame, K., and Silverstein, S. J. (1995). Polyamines alter sequence-specific DNA-protein interactions. Nucleic Acids Res. 23, 1800-1809. doi: 10.1093/nar/23.10.1800
70. Panicot, M., Masgrau, C., Borrell, A., Cordeiro, A., Tiburcio, A. F., and Altabella, T. (2002). Effects of putrescine accumulation in tobacco transgenic plants with different expression levels of oat arginine decarboxylase. Physiol. Plant. 114, 281-287. doi: 10.1034/j.1399-3054.2002.1140214.x
71. Piotrowski, M., Janowitz, T., and Kneifel, H. (2003). Plant C-N hydrolases and the identification of a plant N-carbamoylputrescine amidohydrolase involved in polyamine biosynthesis. J. Biol. Chem. 278, 1708-1712. doi: 10.1074/jbc.M205699200
72. Pottosin, I., Velarde-Buendía, A. M., Bose, J., Zepeda-Jazo, I., Shabala, S., and Dobrovinskaya, O. (2014). Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J. Exp. Bot. 65, 1271-1283. doi: 10.1093/jxb/ert423
73. Pottosin, I., Velarde-Buendía, A.-M., Zepeda-Jazo, I., Dobrovinskaya, O., and Shabala, S. (2012). Synergism between polyamines and ROS in the induction of Ca2+ and K+ fluxes in roots. Plant Signal. Behav. 7, 1084-1087. doi: 10.4161/psb.21185
74. Prakash, L., Dutt, M., and Prathapasenan, G. (1988). NaCl alters contents of nucleic acids, protein, polyamines and the activity of agmatine deiminase during germination and seedling growth of rice (Oryza sativa L.). Funct. Plant Biol. 15, 769-776. doi: 10.1071/PP9880769
75. Prakash, L., and Prathapsenan, G. (1988). Putrescine reduces NaCl-induced inhibition of germination and early seedling growth of rice (Oryza sativa L.). Aust. J. Plant Physiol. 15, 761-767. doi: 10.1071/PP9880761
76. Qadir, M., Tubeileh, A., Akhtar, J., Larbi, A., Minhas, P. S., and Khan, M. A. (2008). Productivity enhancement of salt-affected environments through crop diversification. Land Degradation Dev. 19, 429-453. doi: 10.1002/ldr.853
77. Rabbani, M. A., Maruyama, K., Abe, H., Khan, M. A., Katsura, K., Ito, Y., et al. (2003). Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol. 133, 1755-1767. doi: 10.1104/pp.103.025742
78. Rajam, M. V. (1993). Polyamine biosynthesis inhibitors-new protectants against fungal plant-diseases. Curr. Sci. 65, 461-469.
79. Rajasekaran, L. R., and Blake, T. J. (1999). New plant growth regulators protect photosynthesis and enhance growth under drought of jack pine seedlings. J. Plant Growth Regul. 18, 175-181. doi: 10.1007/PL00007067
80. Ramakers, C., Ruijter, J. M., Deprez, R. H. L., and Moorman, A. F. M. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62-66. doi: 10.1016/S0304-3940(02)01423-4
81. Riadh, K., Wided, M., Hans-Werner, K., and Chedly, A. (2010). "Responses of halophytes to environmental stresses with special emphasis to salinity, " in Advances in Botanical Research, eds J.-C. Kader and M. Delseny (Boston, MA: Elsevier Academic Press), 117-145.
82. Rodríguez-Kessler, M., Alpuche-Solís, A., Ruiz, O., and Jiménez-Bremont, J. (2006). Effect of salt stress on the regulation of maize (Zea mays L.) genes involved in polyamine biosynthesis. Plant Growth Regul. 48, 175-185. doi: 10.1007/s10725-005-5990-4
83. Roy, M., and Wu, R. (2001). Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci. 160, 869-875. doi: 10.1016/S0168-9452(01)00337-5
84. 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. doi: 10.1016/S0168-9452(02)00272-8
85. Roy, P., Niyogi, K., Sengupta, D. N., and Ghosh, B. (2005). Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci. 168, 583-591. doi: 10.1016/j.plantsci.2004.08.014
86. Ruan, C.-J., Da Silva, J. A. T., Mopper, S., Qin, P., and Lutts, S. (2010). Halophyte Improvement for a salinized world. Crit. Rev. Plant Sci. 29, 329-359. doi: 10.1080/07352689.2010.524517
87. Sanchez, D. H., Cuevas, J. C., Chiesa, M. A., and Ruiz, O. A. (2005). Free spermidine and spermine content in Lotus glaber under long-term salt stress. Plant Sci. 168, 541-546. doi: 10.1016/j.plantsci.2004.09.025
88. Shiozaki, N., Yamada, M., and Yoshiba, Y. (2005). Analysis of salt-stress-inducible ESTs isolated by PCR-subtraction in salt-tolerant rice. Theor. Appl. Genet. 110, 1177-1186. doi: 10.1007/s00122-005-1931-x
89. Slocum, R. D. (1991). "Tissue and subcellular localisation of polyamines and enzymes of polyamine metabolism, " in Biochemistry and Physiology of Polyamines in Plants, eds R. D. Slocum and H. E. Flores (Boca Raton, FL: CRC Press), 93-103.
90. Slocum, R. D., Kaur-Sawhney, R., and Galston, A. W. (1984). The physiology and biochemistry of polyamines in plants. Arch. Biochem. Biophys. 235, 283-303. doi: 10.1016/0003-9861(84)90201-7
91. Soyka, S., and Heyer, A. G. (1999). Arabidopsis knockout mutation of ADC2 gene reveals inducibility by osmotic stress. FEBS Lett. 458, 219-223. doi: 10.1016/S0014-5793(99)01125-4
92. Su, J., and Wu, R. (2004). Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci. 166, 941-948. doi: 10.1016/j.plantsci.2003.12.004
93. Tassoni, A., Antognoni, F., Luisa Battistini, M., Sanvido, O., and Bagni, N. (1998). Characterization of spermidine binding to solubilized plasma membrane proteins from zucchini hypocotyls. Plant Physiol. 117, 971-977. doi: 10.1104/pp.117.3.971
94. Tian, A. G., Zhao, J. Y., Zhang, J. S., Gai, J. Y., and Chen, S. Y. (2004). Genomic characterization of the S-adenosylmethionine decarboxylase genes from soybean. Theor. Appl. Genet. 108, 842-850. doi: 10.1007/s00122-003-1507-6
95. Tiburcio, A. F., Altabella, T., Borrell, A., and Masgrau, C. (1997). Polyamine metabolism and its regulation. Physiol. Plant. 100, 664-674. doi: 10.1111/j.1399-3054.1997.tb03073.x
96. Tiburcio, A. F., Kaur-Sawhney, R., and Galston, A. W. (1986). Polyamine metabolism and osmotic stress II. Improvement of oat protoplasts by an inhibitor of arginine decarboxylase. Plant Physiol. 82, 375-378. doi: 10.1104/pp.82.2.375
97. Turner, L. B., and Stewart, G. R. (1986). The effect of water stress upon polyamine levels in barley (Hordeum vulgare L.) leaves. J. Exp. Bot. 37, 170-177. doi: 10.1093/jxb/37.2.170
98. Urano, K., Yoshiba, Y., Nanjo, T., Igarashi, Y., Seki, M., Sekiguchi, F., et al. (2003). Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ. 26, 1917-1926. doi: 10.1046/j.1365-3040.2003.01108.x
99. Urano, K., Yoshiba, Y., Nanjo, T., Ito, T., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2004). Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem. Biophys. Res. Commun. 313, 369-375. doi: 10.1016/j.bbrc.2003.11.119
100. Velarde-Buendía, A. M., Shabala, S., Cvikrova, M., Dobrovinskaya, O., and Pottosin, I. (2012). Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiol. Biochem. 61, 18-23. doi: 10.1016/j.plaphy.2012.09.002
101. Velikova, V. B., Yordanov, I. T., Geogieva, K. M., Tsoney, T. D., and Goltsev, V. (1998). Effects of exogenous polyamines applied separately and in combination with stimulated acid rain on functional activity of photosynthetic apparatus. J. Plant Physiol. 153, 299-307. doi: 10.1016/S0176-1617(98)80155-7
102. Wopereis, M. C. S., Stein, A., Kropff, M. J., and Bouma, J. (1996). Spatial interpolation of soil hydraulic properties and simulated rice yield. Soil Use Manage. 12, 158-166. doi: 10.1111/j.1475-2743.1996.tb00537.x
103. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Takahashi, T., Michael, A. J., et al. (2007). A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem. Biophys. Res. Commun. 352, 486-490. doi: 10.1016/j.bbrc.2006.11.041
104. Yamamoto, A., Shim, I. S., Fujihara, S., Yoneyama, T., and Usui, K. (2004). Effect of difference in nitrogen media on salt-stress response and contents of nitrogen compounds in rice seedlings. Soil Sci. Plant Nutr. 50, 85-93. doi: 10.1080/00380768.2004.10408455
105. Yang, X., Römheld, V., and Marschner, H. (1994). Effect of bicarbonate on root growth and accumulation of organic acids in Zn-inefficient and Zn-efficient rice cultivars (Oryza sativa L.). Plant Soil 164, 1-7. doi: 10.1007/BF00010104
106. Yeo, A. R., Lee, B-S., Izard, P., Boursier, P. J., and Flowers, T. J. (1991). Short-and long-term effects of salinity on leaf growth in rice (Oryza sativa L.). J. Exp. Bot. 42, 881-889. doi: 10.1093/jxb/42.7.881
107. Zhao, F., Song, C.-P., He, J., and Zhu, H. (2007). Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol. 145, 1061-1072. doi: 10.1104/pp.107.105882
108. Zuther, E., Koehl, K., and Kopka, J. (2007). "Comparative metabolome analysis of the salt response in breeding cultivars of rice, " in Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops, eds M. A. Jenks et al. (Dordrecht: Springer Publishing, Inc.), 285-315.