Physiological and molecular implications of plant polyamine metabolism during biotic interactions

Frontiers in Plant Science

Volumn 5, Issue MAR, 2014, Pages

  Jiménez Bremont, Juan F ^a   Marina, María ^b   Guerrero González, María de la Luz ^a   Rossi, Franco R ^b   Sánchez Rangel, Diana ^a   Rodríguez Kessler, Margarita ^c   Ruiz, Oscar A ^d   Gárriz, Andrés ^b  

^a INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^d INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

Mutualism; Plant pathogen; Polyamines; Putrescine; Spermidine; Spermine; Thermospermine

Indexed keywords

EID: 84901063824     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00095     Document Type: Review

References (161)

1. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., et al. (2010). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237-1249. doi: 10.1007/s00425-010-1130-0
2. 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, 815-815. doi: 10.1093/jxb/erm370
3. 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. doi: 10.1016/j.plaphy.2010.02.001
4. Antognoni, F., Casali, P., Pistocchi, R., and Bagni, N. (1994). Kinetics and calcium-specificity of polyamine uptake in carrot protoplasts. Amino Acids 6, 301-309. doi: 10.1007/BF00813750
5. Asthir, B., Spoor, W., and Duffus, C. (2004). Involvement of polyamines, diamine oxidase and polyamine oxidase in resistance of barley to Blumeria graminis f. sp. hordei. Euphytica 136, 307-312. doi: 10.1023/B:EUPH.0000032730.48474.b1
6. Bagni, N., and Tassoni, A. (2001). Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20, 301-317. doi: 10.1007/s007260170046
7. Balint, R., and Cohen, S. S. (1985). The effects of dicyclohexylamine on polyamine biosynthesis and incorporation into turnip yellow mosaic virus in Chinese cabbage protoplasts infected in vitro. Virology 144, 194-203. doi: 10.1016/0042-6822(85)90317-4
8. Belda-Palazón, B., Ruiz, L., Martí, E., Tárraga, S., Tiburcio, A. F., Culiáñez, F., et al. (2012). Aminopropyltransferases involved in polyamine biosynthesis localize preferentially in the nucleus of plant cells. PLoS ONE 7:e46907. doi: 10.1371/journal.pone.0046907
9. Belles, J. M., Carbonell, J., and Conejero, V. (1991). Polyamines in plants infected by citrus exocortis viroid or treated with silver ions and ethephon. Plant Physiol. 96, 1053-1059. doi: 10.1104/pp.96.4.1053
10. Belles, J. M., Perez-Amador, M. A., Carbonell, J., and Conejero, V. (1993). Correlation between ornithine decarboxylase and putrescine in tomato plants infected by citrus exocortis viroid or treated with ethephon. Plant Physiol. 102, 933-937. doi: 10.1104/pp.102.3.933
11. Biondi, S., Fornalé, S., Oksman-Caldentey, K. M., Eeva, M., Agostani, S., and Bagni, N. (2000). Jasmonates induce over-accumulation of methylputrescine and conjugated polyamines in Hyoscyamus muticus L. root cultures. Plant Cell Rep. 19, 691-697. doi: 10.1007/s002999900178
12. Biondi, S., and Scaramagli, S. (2001). Methyl jasmonate upregulates biosynthetic gene expression, oxidation and conjugation of polyamines, and inhibits shoot formation in tobacco thin layers. J. Exp. Bot. 52, 231-242. doi: 10.1093/jexbot/52.355.231
13. Biondi, S., Scoccianti, V., Scaramagli, S., Ziosi, V., and Torrigiani, P. (2003). Auxin and cytokinin modify methyl jasmonate effects on polyamine metabolism and ethylene biosynthesis in tobacco leaf discs. Plant Sci. 165, 95-101. doi: 10.1016/s0168-9452(03)00147-x
14. 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.
15. Bortolotti, C., Cordeiro, A., Alcázar, R., Borrell, A., Culiañez-Macià, F. A., Tiburcio, A. F., et al. (2004). Localization of arginine decarboxylase in tobacco plants. Physiol. Plant. 120, 84-92. doi: 10.1111/j.0031-9317.2004.0216.x
16. Bouche, N., and Fromm, H. (2004). GABA in plants: just a metabolite? Trends Plant Sci. 9, 110-115. doi: 10.1016/j.tplants.2004.01.006
17. Broetto, F., Marchese, J. A., Leonardo, M., and Regina, M. (2005). Fungal elicitor-mediated changes in polyamine content, phenylalanine-ammonia lyase and peroxidase activities in bean cell culture. Gen. Appl. Plant Physiol. 31, 235-246.
18. Cao, S., Cai, Y., Yang, Z., Joyce, D. C., and Zheng, Y. (2014). Effect of MeJA treatment on polyamine, energy status and anthracnose rot of loquat fruit. Food Chem. 145, 86-89. doi: 10.1016/j.foodchem.2013.08.019
19. Carbonell, J., and Blázquez, M. A. (2009). Regulatory mechanisms of polyamine biosynthesis in plants. Genes Genomics 31, 107-118. doi: 10.1007/BF03191144
20. Childs, A. C., Mehta, D. J., and Gerner, E. W. (2003). Polyamine-dependent gene expression. Cell Mol. Life Sci. 60, 1394-1406. doi: 10.1007/s00018-003-2332-4
21. Choi, H. W., and Hwang, B. K. (2012). The pepper extracellular peroxidase CaPO2 is required for salt, drought and oxidative stress tolerance as well as resistance to fungal pathogens. Planta 235, 1369-1382. doi: 10.1007/s00425-011-1580-z
22. Coghlan, S. E., and Walters, D. R. (1990). Polyamine metabolism in "green-islands" on powdery mildew-infected barley leaves: possible interactions with senescence. New Phytol. 116, 417-424. doi: 10.1111/j.1469-8137.1990.tb00527.x
23. Cohen, S. (1998). A Guide to the Polyamines. New York: Oxford University Press.
24. Cona, A., Rea, G., Angelini, R., Federico, R., and Tavladoraki, P. (2006a). Functions of amine oxidases in plant development and defence. Trends Plant Sci. 11, 80-88. doi: 10.1016/j.tplants.2005.12.009
25. Cona, A., Rea, G., Botta, M., Corelli, F., Federico, R., Angelini, R., et al. (2006b). Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. J. Exp. Bot. 57, 2277-2289. doi: 10.1093/jxb/erj195
26. Cowley, T., and Walters, D. R. (2002a). Polyamine metabolism in an incompatible interaction between barley and the powdery mildew fungus, Blumeria graminis f. sp. hordei. J. Phytopathol. 150, 581-586. doi: 10.1046/j.1439-0434.2002.00816.x
27. Cowley, T., and Walters, D. R. (2002b). Polyamine metabolism in barley reacting hypersensitively to the powdery mildew fungus Blumeria graminis f. sp. hordei. Plant Cell Environ. 25, 461-468. doi: 10.1046/j.0016-8025.2001.00819.x
28. D'Agostino, L., Di Pietro, M., and Di Luccia, A. (2005). Nuclear aggregates of polyamines are supramolecular structures that play a crucial role in genomic DNA protection and conformation. FEBS J. 272, 3777-3787. doi: 10.1111/j.1742-4658.2005.04782.x
29. Ditomaso, J. M., Shaff, J. E., and Kochian, L. V. (1989). Putrescine-induced wounding and its effects on membrane integrity and ion transport processes in roots of intact corn seedlings. Plant Physiol. 90, 988-995. doi: 10.1104/pp.90.3.988
30. Efrose, R. C., Flemetakis, E., Sfichi, L., Stedel, C., Kouri, E. D., Udvardi, M. K., et al. (2008). Characterization of spermidine and spermine synthases in Lotus japonicus: induction and spatial organization of polyamine biosynthesis in nitrogen fixing nodules. Planta 228, 37-49. doi: 10.1007/s00425-008-07171
31. El Ghachtouli, N., Paynot, M., Morandi, D., Martin-Tanguy, J., and Gianinazzi, S. (1995). The effect of polyamines on endomycorrhizal infection of wild-type Pisum sativum, cv. Frisson (nod+ myc+) and two mutants (nod-myc+ and nod-myc-). Mycorrhiza 5, 189-192. doi: 10.1007/bf00203336
32. Federico, R., and Angelini, R. (1991). "Polyamine catabolism in plants, " in Biochemistry and Physiology of Polyamines in Plants, eds R. D. Slocum and H. E. Flores (Boca Raton, FL: CRC Press), 41-56.
33. Fincato, P., Moschou, P. N., Spedaletti, V., Tavazza, R., Angelini, R., Federico, R., et al. (2011). Functional diversity inside the Arabidopsis polyamine oxidase gene family. J. Exp. Bot. 62, 1155-1168. doi: 10.1093/jxb/erq341
34. Flemetakis, E., Efrose, R. C., Desbrosses, G., Dimou, M., Delis, C., Aivalakis, G., et al. (2004). Induction and spatial organization of polyamine biosynthesis during nodule development in Lotus japonicus. Mol. Plant Microbe Interact. 17, 1283-1293. doi: 10.1094/mpmi.2004.17.12.1283
35. Foster, S. A., and Walters, D. R. (1992). Polyamine concentrations and activities of ornithine and arginine decarboxylase in wheat infected with the stem rust fungus. J. Plant Physiol. 140, 134-136. doi: 10.1016/S0176-1617(11)80922-3
36. Friedman, R., Levin, N., and Altman, A. (1986). Presence and identification of polyamines in xylem and Phloem exudates of plants. Plant Physiol. 82, 1154-1157. doi: 10.1104/pp.82.4.1154
37. Fu, X. Z., Chen, C. W., Wang, Y., Liu, J. H., and Moriguchi, T. (2011). Ectopic expression of MdSPDS1 in sweet orange (Citrus sinensis Osbeck) reduces canker susceptibility: involvement of H(2)O(2) production and transcriptional alteration. BMC Plant Biol. 11:55. doi: 10.1186/1471-2229-1155
38. Fu, X.-Z., and Liu, J.-H. (2013). Transcriptional profiling of canker-resistant transgenic sweet orange (Citrus sinensis Osbeck) constitutively overexpressing a spermidine synthase. Biomed. Res. Int. 2013. doi: 10.1155/2013/918136
39. Fuell, C., Elliott, K. A., Hanfrey, C. C., Franceschetti, M., and Michael, A. J. (2010). Polyamine biosynthetic diversity in plants and algae. Plant Physiol. Biochem. 48, 513-520. doi: 10.1016/j.plaphy.2010.02.008
40. Fujihara, S. (2009). Biogenic amines in rhizobia and legume root nodules. Microbes Environ. 24, 1-13. doi: 10.1264/jsme2.ME08557
41. Fujihara, S., Abe, H., Minakawa, Y., Akao, S., and Yoneyama, T. (1994). Polyamines in nodules from various plant-microbe symbiotic associations. Plant Cell Physiol. 35, 1127-1134.
42. Fujihara, S., Nakashima, T., Kurogochi, Y., and Yamaguchi, M. (1986). Distribution and metabolism of sym-homospermidine and canavalmine in the sword bean Canavalia gladiata cv shironata. Plant Physiol. 82, 795-800. doi: 10.1104/pp.82.3.795
43. Fujihara, S., and Yoneyama, T. (1999). "Polyamine metabolism of root nodule bacteria, " in Recent Research Development in Microbiology, ed. S. G. Pandalai (India: Research Singpost), 55-80.
44. Fujita, M., Fujita, Y., Iuchi, S., Yamada, K., Kobayashi, Y., Urano, K., et al. (2012). Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 6343-6347. doi: 10.1073/pnas.1121406109
45. Galloway, G. L., Malmberg, R. L., and Price, R. A. (1998). Phylogenetic utility of the nuclear gene arginine decarboxylase: an example from Brassicaceae. Mol. Biol. Evol. 15, 1312-1320. doi: 10.1093/oxfordjournals.molbev.a025859
46. Ge, C., Cui, X., Wang, Y., Hu, Y., Fu, Z., Zhang, D., et al. (2006). BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res. 16, 446-456. doi: 10.1038/sj.cr.7310056
47. 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
48. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227. doi: 10.1146/annurev.phyto.43.040204.135923
49. Gonzalez, M. E., Marco, F., Minguet, E. G., Carrasco-Sorli, P., Blázquez, M. A., Carbonell, J., et al. (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. doi: 10.1104/pp.110.171413
50. Govrin, E. M., and Levine, A. (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751-757. doi: 10.1016/S0960-9822(00)00560-1
51. Greenland, A. J., and Lewis, D. H. (1984). Amines in barley leaves infected by brown rust and their possible relevance to formation of "green islands". New phytol. 96, 283-291. doi: 10.1111/j.1469-8137.1984.tb03565.x
52. Guerrero-González, M. L., Rodriguez-Kessler, M., and Jimenez-Bremont, J. F. (2014). uORF, a regulatory mechanism of the Arabidopsis polyamine oxidase 2. Mol. Biol. Rep. doi: 10.1007/s11033-014-3098-5 [Epub ahead of print].
53. Haggag, W. M., and Abd-El-Kareem, F. (2009). Methyl jasmonate stimulates polyamines biosynthesisand resistance against leaf rust in wheat plants. Arch. Phytopathol. Plant Protect. 42, 16-31. doi: 10.1080/03235400600914355
54. Hanfrey, C., Franceschetti, M., Mayer, M. J., Illingworth, C., Elliott, K., Collier, M., et al. (2003). Translational regulation of the plant S-adenosylmethionine decarboxylase. Biochem. Soc. Trans. 31, 424-427. doi: 10.1042/BST0310424
55. Hanfrey, C., Franceschetti, M., Mayer, M. J., Illingworth, C., and Michael, A. J. (2002). Abrogation of upstream open reading frame-mediated translational control of a plant S-adenosylmethionine decarboxylase results in polyamine disruption and growth perturbations. J. Biol. Chem. 277, 44131-44139. doi: 10.1074/jbc.M206161200
56. Hanfrey, C., Sommer, S., Mayer, M. J., Burtin, D., and Michael, A. J. (2001). Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J. 27, 551-560. doi: 10.1046/j.1365-313X.2001.01100.x
57. Hazarika, P., and Rajam, M. V. (2011). Biotic and abiotic stress tolerance in transgenic tomatoes by constitutive expression of S-adenosylmethionine decarboxylase gene. Physiol. Mol. Biol. Plants 17, 115-128. doi: 10.1007/s12298-011-0053-y
58. He, Y., Kashiwagi, K., Fukuchi, J., Terao, K., Shirahata, A., and Igarashi, K. (1993). Correlation between the inhibition of cell growth by accumulated polyamines and the decrease of magnesium and ATP. Eur. J. Biochem. 217, 89-96. doi: 10.1111/j.1432-1033.1993.tb18222.x
59. Hewezi, T., Howe, P. J., Maier, T. R., Hussey, R. S., Mitchum, M. G., Davis, E. L., et al. (2010). Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol. 152, 968-984. doi: 10.1104/pp.109.150557
60. Hummel, I., Bourdais, G., Gouesbet, G., Couée, I., Malmberg, R. L., and Amrani, A. E. (2001). Differential gene expression of ARGININE DECARBOXYLASE ADC1 and ADC2 in Arabidopsis thaliana: characterization of transcriptional regulation during seed germination and seedling development. New Phytol. 519-531. doi: 10.1111/j.1469-8137.2004.01128.x
61. Hummel, I., Gouesbet, G., El Amrani, A., Aínouche, A., and Couée, I. (2004). Characterization of the two arginine decarboxylase (polyamine biosynthesis) paralogues of the endemic subantarctic cruciferous species Pringlea antiscorbutica and analysis of their differential expression during development and response to environmental stress. Gene 342, 199-209. doi: 10.1016/j.gene.2004.08.024
62. 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
63. Igarashi, K., and Kashiwagi, K. (2000). Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun. 271, 559-564. doi: 10.1006/bbrc.2000.2601
64. Igarashi, K., and Kashiwagi, K. (2010). Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol. Biochem. 48, 506-512. doi: 10.1016/j.plaphy.2010.01.017
65. Imai, A., Akiyama, T., Kato, T., Sato, S., Tabata, S., Yamamoto, K. T., et al. (2004a). Spermine is not essential for survival of Arabidopsis. DNA Res. 556, 148-152. doi: 10.1016/s0014-5793(03)01395-4
66. Imai, A., Matsuyama, T., Hanzawa, Y., Akiyama, T., Tamaoki, M., Saji, H., et al. (2004b). Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol. 135, 1565-1573. doi: 10.1104/pp.104.041699
67. Jang, E.-K., Min, K.-H., Kim, S.-H., Nam, S.-H., Zhang, S., Kim, Y. C., et al. (2009). Mitogen-activated protein kinase cascade in the signaling for polyamine biosynthesis in tobacco. Plant Cell Physiol. 50, 658-664. doi: 10.1093/pcp/pcp009
68. Jiménez-Bremont, J. F., Camacho-Villasana, Y. M., Cabrera-Ponce, J. L., De La Rosa, A. P. B., and Ochoa-Alejo, N. (2004). Sequence comparison of plant ornithine decarboxylases reveals high homology and lack of introns. Biol. Plant. 48, 193-198. doi: 10.1023/B:BIOP.0000033444.17603.f2
69. Jimenez-Bremont, J. F., Ruiz, O. A., and Rodriguez-Kessler, M. (2007). Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol. Biochem. 45, 812-821. doi: 10.1016/j.plaphy.2007.08.001
70. Jubault, M., Hamon, C., Gravot, A., Lariagon, C., Delourme, R., Bouchereau, A., et al. (2008). Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiol. 146, 2008-2019. doi: 10.1104/pp.108.117432
71. Kamada-Nobusada, T., Hayashi, M., Fukazawa, M., Sakakibara, H., and Nishimura, M. (2008). A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol. 49, 1272-1282. doi: 10.1093/pcp/pcn114
72. Kaur, H., Heinzel, N., Schottner, M., Baldwin, I. T., and Galis, I. (2010). R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol. 152, 1731-1747. doi: 10.1104/pp.109.151738
73. Kim, N. H. D., Kim, B. S. D., and Hwang, B. K. D. (2013a). Pepper arginine decarboxylase is required for polyamine and gamma-aminobutyric acid signaling in cell death and defense response. Plant Physiol. 162, 2067-2083. doi: 10.1104/pp.113.217372
74. Kim, S. H., Yoo, S. J., Min, K. H., Nam, S. H., Cho, B. H., and Yang, K. Y. (2013b). Putrescine regulating by stress-responsive MAPK cascade contributes to bacterial pathogen defense in Arabidopsis. Biochem. Biophys. Res. Commun. 437, 502-508. doi: 10.1016/j.bbrc.2013.06.080
75. Kusano, T., Yamaguchi, K., Berberich, T., and Takahashi, Y. (2007). Advances in polyamine research in 2007. J. Plant Res. 120, 345-350. doi: 10.1007/s10265-007-0074-3
76. Kytöviita, M.-M., and Sarjala, T. (1997). Effects of defoliation and symbiosis on polyamine levels in pine and birch. Mycorrhiza 7, 107-111. doi: 10.1007/s005720050170
77. Lazzarato, L., Trebbi, G., Pagnucco, C., Franchin, C., Torrigiani, P., and Betti, L. (2009). Exogenous spermidine, arsenic and-aminobutyric acid modulate tobacco resistance to tobacco mosaic virus, and affect local and systemic glucosylsalicylic acid. J. Plant Physiol. 166, 90-100. doi: 10.1016/j.jplph.2008.01.011
78. Legaz, M. E., Armas, R. D., Piñon, D., and Vicente, C. (1998). Relationships between phenolics-conjugated polyamines and sensitivity of sugarcane to smut (Ustilago scitaminea). J. Exp. Bot. 49, 1723-1728. doi: 10.1093/jxb/49.327.1723
79. López-Gómez, M., Hidalgo-Castellanos, J., Iribarne, C., and Lluch, C. (2014). Proline accumulation has prevalence over polyamines in nodules of Medicago sativa in symbiosis with Sinorhizobium meliloti during the initial response to salinity. Plant Soil 374, 149-159. doi: 10.1007/s11104-013-1871-1
80. Machatschke, S., Kamrowski, C., Moerschbacher, B. M., and Reisener, H.-J. (1990). Polyamine levels in stem rust infected wheat leaves and effects of alpha-difluoromethylornithine on fungal infection. Physiol. Mol. Plant Pathol. 36, 451-459. doi: 10.1016/0885-5765(90)90018-S
81. Mackintosh, C. A., Slater, L. A., Mcclintock, C. A., Walters, D. R., Havis, N. D., and Robins, D. J. (1997). Synthesis and antifungal activity of two novel spermidine analogues. FEMS Microbiol. Lett. 148, 21-25. doi: 10.1111/j.1574-6968.1997.tb10261.x
82. Marina, M., Maiale, S. J., Rossi, F. R., Romero, M. F., Rivas, M. E., Gárriz, A., et al. (2008). Apoplastic polyamine oxidation oxidation plays different roles in local responses of tobacco to infection by the necrotrophic fungus Sclerotinia sclerotiorum and the biotrophic bacterium Pseudomonas. Plant Physiol. 147, 2164-2178. doi: 10.1104/pp.108.122614
83. Marina, M., Sirera, F. V., Rambla, J. L., Gonzalez, M. E., Blázquez, M. A., Carbonell, J., et al. (2013). Thermospermine catabolism increases Arabidopsis thaliana resistance to Pseudomonas viridiflava. J. Exp. Bot. 64, 1393-1402. doi: 10.1093/jxb/ert012
84. Marini, F., Betti, L., Scaramagli, S., Biondi, S., and Torrigiani, P. (2001). Polyamine metabolism is upregulated in response to tobacco mosaic virus in hypersensitive, but not in susceptible tobacco. New Phytol. 149, 301-309. doi: 10.2307/3186182
85. 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
86. Martin-Tanguy, J., Martin, C., Gallet, M., and Vernoy, R. (1976). Potent natural inhibitors of tobacco mosaic virus multiplication. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 282, 2231-2234.
87. Mattoo, A. K., Minocha, S. C., Minocha, R., and Handa, A. K. (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
88. Mendes, R., Garbeva, P., and Raaijmakers, J. M. (2013). The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634-663. doi: 10.1111/1574-6976.12028
89. Mitsuya, Y., Takahashi, Y., Uehara, Y., Berberich, T., Miyazaki, A., Takahashi, H., et al. (2007). Identification of a novel Cys 2/His 2-type zinc-finger protein as a component of a spermine-signaling pathway in tobacco. J. Plant Physiol. 164, 785-793. doi: 10.1016/j.jplph.2006.05.011
90. Moschou, P. N., Paschalidis, K. A., Delis, I. D., Andriopoulou, A. H., Lagiotis, G. D., Yakoumakis, D. I., et al. (2008a). 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. doi: 10.1105/tpc.108.059733
91. Moschou, P. N., Paschalidis, K. A., and Roubelakis-Angelakis, K. A. (2008b). Plant polyamine catabolism: the state of the art. Plant Signal. Behav. 3, 1061-1066. doi: 10.4161/psb.3.12.7172
92. Moschou, P. N., Sanmartin, M., Andriopoulou, A. H., Rojo, E., Sanchez-Serrano, J. J., and Roubelakis-Angelakis, K. A. (2008c). Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol. 147, 1845-1857. doi: 10.1104/pp.108.123802
93. Moschou, P. N., Sarris, P. F., Skandalis, N., Andriopoulou, A. H., Paschalidis, K. A., Panopoulos, N. J., et al. (2009). Engineered polyamine catabolism preinduces tolerance of tobacco to bacteria and oomycetes. Plant Physiol. 149, 1970-1981. doi: 10.1104/pp.108.134932
94. Mulangi, V., Chibucos, M. C., Phuntumart, V., and Morris, P. F. (2012a). Kinetic and phylogenetic analysis of plant polyamine uptake transporters. Planta 236, 1261-1273. doi: 10.1007/s00425-012-1668-0
95. Mulangi, V., Phuntumart, V., Aouida, M., Ramotar, D., and Morris, P. (2012b). Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235, 1-11. doi: 10.1007/s00425-011-1486-9
96. Muroi, A., Ishihara, A., Tanaka, C., Ishizuka, A., Takabayashi, J., Miyoshi, H., and Nishioka, T. (2009). Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in Arabidopsis thaliana. Planta 230, 517-527. doi: 10.1007/s00425-009-0960-960.
97. Nambeesan, S., Abuqamar, S., Laluk, K., Mattoo, A. K., Mickelbart, M. V., Ferruzzi, M. G., et al. (2012). Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol. 158, 1034-1045. doi: 10.1104/pp.111.188698
98. Nanda, A. K., Andrio, E., Marino, D., Pauly, N., and Dunand, C. (2010). Reactive oxygen species during plant-microorganism early interactions. J. Integr. Plant Biol. 52, 195-204. doi: 10.1111/j.1744-7909.2010.00933.x
99. Németh, M., Janda, T., Horváth, E., Páldi, E., and Szalai, G. (2002). Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci. 162, 569-574. doi: 10.1016/S0168-9452(01)00593-3
100. Niemi, K., Haggman, H., and Sarjala, T. (2002). Effects of exogenous diamines on the interaction between ectomycorrhizal fungi and adventitious root formation in Scots pine in vitro. Tree Physiol. 22, 373-381. doi: 10.1093/treephys/22.6.373
101. Niemi, K., Sutela, S., Häggman, H., Scagel, C., Vuosku, J., Jokela, A., et al. (2006). Changes in polyamine content and localization of Pinus sylvestris ADC and Suillus variegatus ODC mRNA transcripts during the formation of mycorrhizal interaction in an in vitro cultivation system. J. Exp. Bot. 57, 2795-2804. doi: 10.1093/jxb/erl049.
102. Oldroyd, G. E., and Downie, J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546. doi: 10.1146/annurev.arplant.59.032607.092839
103. Onkokesung, N., Gaquerel, E., Kotkar, H., Kaur, H., Baldwin, I. T., and Galis, I. (2012). MYB8 controls inducible phenolamide levels by activating three novel hydroxycinnamoyl-coenzyme A: polyamine transferases in Nicotiana attenuata. Plant Physiol. 158, 389-407. doi: 10.1104/pp.111.187229
104. Ono, Y., Kim, D. W., Watanabe, K., Sasaki, A., Niitsu, M., Berberich, T., et al. (2012). Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino Acids 42, 867-876. doi: 10.1007/s00726-011-1002-3
105. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775. doi: 10.1038/nrmicro1987
106. Paschalidis, K. A., and Roubelakis-Angelakis, K. A. (2005). Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant. Correlations with age, cell division/expansion, and differentiation. Plant Physiol. 138, 142-152. doi: 10.1104/pp.104.055483
107. Peremarti, A., Bassie, L., Yuan, D., Pelacho, A., Christou, P., and Capell, T. (2010). Transcriptional regulation of the rice arginine decarboxylase (Adc1) and S-denosylmethionine decarboxylase (Samdc) genes by methyl jasmonate. Plant Physiol. Biochem. 48, 553-559. doi: 10.1016/j.plaphy.2010.01.014
108. Perez-Amador, M. A., Leon, J., Green, P. J., and Carbonell, J. (2002). Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol. 130, 1454-1463. doi: 10.1104/pp.009951.mechanism
109. Pistocchi, R., Keller, F., Bagni, N., and Matile, P. (1988). Transport and subcellular localization of polyamines in carrot protoplasts and vacuoles. Plant Physiol. 87, 514-518. doi: 10.1104/pp.87.2.514
110. Planas-Portell, J., Gallart, M., Tiburcio, A. F., and Altabella, T. (2013). Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol. 13:109. doi: 10.1186/1471-2229-13-109
111. Poulin, R., Coward, J. K., Lakanen, J. R., and Pegg, A. E. (1993). Enhancement of the spermidine uptake system and lethal effects of spermidine overaccumulation in ornithine decarboxylase-overproducing L1210 cells under hyposmotic stress. J. Biol. Chem. 268, 4690-4698.
112. Prabhavathi, V. R., and Rajam, M. V. (2007). Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol. J. 24, 273-282. doi: 10.5511/plantbiotechnology.24.273
113. Raju, S., Jayalakshmi, S. K., and Sreeramulu, K. (2009). Differential elicitation of proteases and protease inhibitors in two different genotypes of chickpea (Cicer arietinum) by salicylic acid and spermine. J. Plant Physiol. 166, 1015-1022. doi: 10.1016/j.jplph.2008.12.005
114. Rea, G., Metoui, O., Infantino, A., Federico, R., and Angelini, R. (2002). Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiol. 128, 865-875. doi: 10.1104/pp.010646
115. Rea, G., Pinto, M. C. D., Tavazza, R., and Biondi, S. (2004). Ectopic expression of maize polyamine oxidase and pea copper amine oxidase in the cell wall of tobacco plants. Plant 134, 1414-1426. doi: 10.1104/pp.103.036764.of
116. Rodriguez-Kessler, M., Ruiz, O. A., Maiale, S., Ruiz-Herrera, J., and Jimenez-Bremont, J. F. (2008). Polyamine metabolism in maize tumors induced by Ustilago maydis. Plant Physiol. Biochem. 46, 805-814. doi: 10.1016/j.plaphy.2008.05.012
117. Ruiz-Herrera, J., Ruiz-Medrano, R., and Dominguez, A. (1995). Selective inhibition of cytosine-DNA methylases by polyamines. FEBS Lett. 357, 192-196. doi: 10.1016/0014-5793(94)01360-D
118. Sagor, G. H. M., Cong, R.-Z., Berberich, T., Takahashi, H., Takahashi, Y., and Kusano, T. (2009). Spermine signaling in defense reaction against avirulent viral pathogen in Arabidopsis thaliana. Plant Signal. Behav. 4, 316-318. doi: 10.1016/j.jplph.2008.08.006.Polyamines
119. Sagor, G. H. M., Liu, T., Takahashi, H., Niitsu, M., Berberich, T., and Kusano, T. (2013). Longer uncommon polyamines have a stronger defense gene-induction activity and a higher suppressing activity of Cucumber mosaic virus multiplication compared to that of spermine in Arabidopsis thaliana. Plant Cell Rep. 32, 1477-1488. doi: 10.1007/s00299-013-1459-5
120. Sagor, G. H. M., Takahashi, H., Niitsu, M., Takahashi, Y., Berberich, T., and Kusano, T. (2012). Exogenous thermospermine has an activity to induce a subset of the defense genes and restrict cucumber mosaic virus multiplication in Arabidopsis thaliana. Plant Cell Rep. 31, 1227-1232. doi: 10.1007/s00299-012-1243-y
121. Sannazzaro, A. I., Echeverria, M., Alberto, E. O., Ruiz, O. A., and Menendez, A. B. (2007). Modulation of polyamine balance in Lotus glaber by salinity and arbuscular mycorrhiza. Plant Physiol. Biochem. 45, 39-46. doi: 10.1016/j.plaphy.2006.12.008
122. Šebela, M., Radová, A., and Angelini, R. (2001). FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Sci. 160, 197-207. doi: 10.1016/S0168-9452(00)00380-0
123. Stes, E., Biondi, S., Holsters, M., and Vereecke, D. (2011). Bacterial and plant signal integration via D3-type cyclins enhances symptom development in the Arabidopsis-Rhodococcus fascians interaction. Plant Physiol. 156, 712-725. doi: 10.1104/pp.110.171561
124. Sulieman, S. (2011). Does GABA increase the efficiency of symbiotic N2 fixation in legumes? Plant Signal. Behav. 6, 32-36.
125. Sulieman, S., and Schulze, J. (2010). Phloem-derived gamma-aminobutyric acid (GABA) is involved in upregulating nodule N2 fixation efficiency in the model legume Medicago truncatula. Plant Cell Environ. 33, 2162-2172. doi: 10.1111/j.1365-3040.2010.02214.x
126. Takahashi, Y., Berberich, T., Miyazaki, A., Seo, S., Ohashi, Y., and Kusano, T. (2003). Spermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J. 36, 820-829. doi: 10.1046/j.1365-313X.2003.01923.x
127. Takahashi, Y., Berberich, T., Yamashita, K., and Uehara, Y. (2004a). Identification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf-and flower-senescence. Plant Mol. Biol. 54, 613-622. doi: 10.1023/B:PLAN.0000038276.95539.39
128. Takahashi, Y., Uehara, Y., Berberich, T., Ito, A., Saitoh, H., Miyazaki, A., et al. (2004b). A subset of hypersensitive response marker genes, including HSR203J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J. 40, 586-595. doi: 10.1111/j.1365-313X.2004.02234.x
129. Takahashi, Y., Cong, R., Sagor, G. H. M., Niitsu, M., Berberich, T., and Kusano, T. (2010). Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep. 29, 955-965. doi: 10.1007/s00299-010-0881-1
130. Tang, W., and Newton, R. J. (2005). Polyamines promote root elongation and growth by increasing root cell division in regenerated Virginia pine (Pinus virginiana Mill) plantlets. Plant Cell Rep. 24, 581-589. doi: 10.1007/s00299-005-0021-5
131. Tavladoraki, P., Rossi, M. N., Saccuti, G., Perez-Amador, M. A., Polticelli, F., Angelini, R., et al. (2006). Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol. 141, 1519-1532. doi: 10.1104/pp.106.080911.caldohexamine
132. Tavladoraki, P., Schinina, M. E., Cecconi, F., Di Agostino, S., Manera, F., Rea, G., et al. (1998). Maize polyamine oxidase: primary structure from protein and cDNA sequencing. FEBS Lett. 426, 62-66. doi: 10.1016/S0014-5793(98)00311-1
133. Terakado, J., Yoneyama, T., and Fujihara, S. (2006). Shoot-applied polyamines suppress nodule formation in soybean (Glycine max). J. Plant Physiol. 163, 497-505. doi: 10.1016/j.jplph.2005.05.007
134. Tomar, P. C., Lakra, N., and Mishra, S. (2013). Cadaverine: a lysine catabolite involved in plant growth and development. Plant Signal. Behav. 8. doi: 10.4161/psb.25850
135. Torrigiani, P., Scaramagli, S., Ziosi, V., Mayer, M., and Biondi, S. (2005). Expression of an antisense Datura stramonium S-adenosylmethionine decarboxylase cDNA in tobacco: changes in enzyme activity, putrescine-spermidine ratio, rhizogenic potential, and response to methyl jasmonate. J. Plant Physiol. 162, 559-571. doi: 10.1016/j.jplph.2004.10.008
136. Torrigiani, P., Serafini-Fracassini, D., Biondi, S., and Bagni, N. (1986). Evidence for the subcellular localization of polyamines and their biosynthetic enzymes in plant cells. J. Plant Physiol. 124, 23-29. doi: 10.1016/S0176-1617(86)80174-2
137. Urano, K., Hobo, T., and Shinozaki, K. (2005). Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett. 579, 1557-1564. doi: 10.1016/j.febslet.2005.01.048
138. Vassileva, V., and Ignatov, G. (1999). Polyamine-induced changes in symbiotic parameters of the Galega orientalis-Rhizobium galegae nitrogen-fixing system. Plant Soil 210, 83-91. doi: 10.1023/a:1004636800869
139. Waie, B., and Rajam, M. V. (2003). Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci. 164, 727-734. doi: 10.1016/s0168-9452(03)00030-x
140. Wallace, H. M., Fraser, A. V., and Hughes, A. (2003). A perspective of polyamine metabolism. Biochem. J. 376, 1-14. doi: 10.1042/BJ20031327
141. Walters, D. R. (2003). Polyamines and plant disease. Phytochemistry 64, 97-107. doi: 10.1016/S0031-9422(03)00329-7
142. Walters, D., Cowley, T., and Mitchell, A. (2002). Methyl jasmonate alters polyamine metabolism and induces systemic protection against powdery mildew infection in barley seedlings. J. Exp. Bot. 53, 747-756. doi: 10.1093/jexbot/53.369.747
143. Walters, D., Meurer-Grimes, B., and Rovira, I. (2001). Antifungal activity of three spermidine conjugates. FEMS Microbiol. Lett. 201, 255-258. doi: 10.1111/j.1574-6968.2001.tb10765.x
144. Walters, D. R., and Shuttleton, M. A. (1985). Polyamines in the roots of turnip infected with Plasmodiophora brassicae Wor. New Phytol. 100, 209-214. doi: 10.1111/j.1469-8137.1985.tb02772.x
145. Walters, D. R., Wilson, P. W. F., and Shuttleton, M. A. (1985). Changes in levels of polyamines and activities of their biosynthetic enzymes in barley infected with the powdery mildew fungus, Erysiphe graminis DC ex Merat f. sp. New Phytol. 101, 695-705. doi: 10.1111/j.1469-8137.1985.tb02875.x
146. Walters, D. R., and Wylie, M. A. (1986). Polyamines in discrete regions of barley leaves infected with the powdery mildew fungus, Erysiphe graminis. Physiol. Plant. 67, 630-633. doi: 10.1111/j.1399-3054.1986.tb05068.x
147. Wimalasekera, R., Tebartz, F., and Scherer, G. F. E. (2011a). Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci. 181, 593-603. doi: 10.1016/j.plantsci.2011.04.002
148. Wimalasekera, R., Villar, C., Begum, T., and Scherer, G. F. E. (2011b). 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. doi: 10.1093/mp/ssr023
149. Wisniewski, J. P., and Brewin, N. J. (2000). Construction of transgenic pea lines with modified expression of diamine oxidase and modified nodulation responses with exogenous putrescine. Mol. Plant Microbe Interact. 13, 922-928. doi: 10.1094/MPMI.2000.13.9.922
150. Wisniewski, J. P., Rathbun, E. A., Knox, J. P., and Brewin, N. J. (2000). Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol. Plant Microbe Interact. 13, 413-420. doi: 10.1094/MPMI.2000.13.4.413
151. Wu, Q.-S., and Zou, Y.-N. (2009). The effect of dual application of arbuscular mycorrhizal fungi and polyamines upon growth and nutrient uptake on trifoliate orange (Poncirus trifoliata) seedlings. Not. Bot. Horti. Agrobot. Cluj Napoca 37.
152. Wu, Q.-S., Zou, Y.-N., Liu, C.-Y., and Lu, T. (2012). Interacted effect of abuscular mycorrhizal fungi and polyamines on root system architecture of Citrus seedlings. J. Integr. Agric. 11, 1675-1681. doi: 10.1016/S2095-3119(12)60170-1
153. Xu, B., Sheehan, M., and Timko, M. (2004). Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. Bright Yellow 2) cell suspensions by methyl-jasmonate treatment. Plant Growth Regul. 44, 101-116. doi: 10.1023/B:GROW.0000049419.22779.f5
154. Yamakawa, H., Kamada, H., Satoh, M., and Ohashi, Y. (1998). Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus. Plant Physiol. 118, 1213-1222. doi: 10.1104/pp.118.4.1213
155. Yao, Q., Wang, L.-R., Xing, Q.-X., Chen, J.-Z., and Zhu, H.-H. (2010). Exogenous polyamines influence root morphogenesis and arbuscular mycorrhizal development of Citrus limonia seedlings. Plant Growth Regul. 60, 27-33. doi: 10.1007/s10725-009-9415-7
156. Yoda, H., Fujimura, K., Takahashi, H., Munemura, I., Uchimiya, H., and Sano, H. (2009). Polyamines as a common source of hydrogen peroxide in host-and nonhost hypersensitive response during pathogen infection. Plant Mol. Biol. 70, 103-112. doi: 10.1007/s11103-009-9459-0
157. 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. doi: 10.1104/pp.106.080515
158. Yoda, H., Yamaguchi, Y., and Sano, H. (2003). Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol. 132, 1973-1981. doi: 10.1104/pp.103.024737.Polyamines
159. Zhang, X., Shen, L., Li, F., Meng, D., and Sheng, J. (2011a). Methyl salicylate-induced arginine catabolism is associated with up-regulation of polyamine and nitric oxide levels and improves chilling tolerance in cherry tomato fruit. J. Agr. Food Chem. 59, 9351-9357. doi: 10.1021/jf201812r
160. Zhang, Z., Chen, H., Huang, X., Xia, R., Zhao, Q., Lai, J., et al. (2011b). BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23, 273-288. doi: 10.1105/tpc.110.081695
161. Zheng, M. S., Takahashi, H., Miyazaki, A., Yamaguchi, K., and Kusano, T. (2005). Identification of the cis-acting elements in Arabidopsis thaliana NHL10 promoter responsible for leaf senescence, the hypersensitive response against Cucumber mosaic virus infection, and spermine treatment. Plant Sci. 168, 415-422. doi: 10.1016/j.plantsci.2004.09.016