Global metabolic profiling of arabidopsis polyamine oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence

Frontiers in Plant Science

Volumn 7, Issue FEB2016, 2016, Pages

  Sequera Mutiozabal, Miren I ^a   Erban, Alexander ^b   Kopka, Joachim ^b   Atanasov, Kostadin E ^a   Bastida, Jaume ^a   Fotopoulos, Vasileios ^c   Alcázar, Rubén ^a   Tiburcio, Antonio F ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

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

^c CYPRUS UNIVERSITY OF TECHNOLOGY   (Cyprus)

Author keywords

Arabidopsis; Oxidative stress; Polyamine oxidases; Polyamines; Senescence; Spermine

Indexed keywords

EID: 84960106242     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00173     Document Type: Article

References (100)

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. Allwood, J. W., De Vos, R. C. H., Moing, A., Deborde, C., Erban, A., Kopka, J., et al. (2011). Plant metabolomics and its potential for systems biology research: background concepts, technology, and methodology. Methods Enzymol. 500, 299-336. doi: 10.1016/B978-0-12-385118-5.00016-5
3. 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, 815-825. doi: 10.1093/jxb/erm370
4. 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
5. Araújo, W. L., Ishizaki, K., Nunes-Nesi, A., Larson, T. R., Tohge, T., Krahnert, I., et al. (2010). Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain ofArabidopsis mitochondria. Plant Cell 22, 1549-1563. doi: 10.1105/tpc.110.075630
6. Araújo, W. L., Tohge, T., Ishizaki, K., Leaver, C. J., and Fernie, A. R. (2011). Protein degradation - an alternative respiratory substrate for stressed plants. Trends Plant Sci.16, 489-498. doi: 10.1016/j.tplants.2011.05.008
7. Bhatnagar, P., Minocha, R., and Minocha, S. C. (2002). Genetic Manipulation of the metabolism of polyamines in poplar cells. the regulation of putrescine catabolism. Plant Physiol. 128, 1455-1469. doi: 10.1104/pp.010792.1
8. 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
9. Bouché, N., Lacombe, B., and Fromm, H. (2003). GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol. 13, 607-610. doi: 10.1016/j.tcb.2003.10.001
10. Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Pyung, O. L., Hong, G. N., et al. (2005). Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42, 567-585. doi: 10.1111/j.1365-313X.2005.02399.x
11. Cai, G., Sobieszczuk-Nowicka, E., Aloisi, I., Fattorini, L., Serafini-Fracassini, D., and Del Duca, S. (2014). Polyamines are common players in different facets of plant programmed cell death. Amino Acids 47, 27-44. doi: 10.1007/s00726-014-1865-1
12. Chae, L., Lee, I., Shin, J., and Rhee, S. Y. (2012). Towards understanding how molecular networks evolve in plants. Curr. Opin. Plant Biol. 15, 177-184. doi: 10.1016/j.pbi.2012.01.006
13. Cona, A., Rea, G., Angelini, R., Federico, R., and Tavladoraki, P. (2006). Functions of amine oxidases in plant development and defence. Trends Plant Sci. 11, 80-88. doi: 10.1016/j.tplants.2005.12.009
14. Corpas, F. J., and Barroso, J. B. (2014). Peroxynitrite (ONOO-) is endogenously produced in arabidopsis peroxisomes and is overproduced under cadmium stress.Ann. Bot. 113, 87-96. doi: 10.1093/aob/mct260
15. Corpas, F. J., Hayashi, M., Mano, S., Nishimura, M., and Barroso, J. B. (2009). Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol. 151, 2083-2094. doi: 10.1104/pp.109.146100
16. Del Duca, S., Serafini-Fracassini, D., and Cai, G. (2014). Senescence and programmed cell death in plants: polyamine action mediated by transglutaminase. Front. Plant Sci.5:120. doi: 10.3389/fpls.2014.00120
17. Diaz, C., Purdy, S., Christ, A., Morot-Gaudry, J.-F., Wingler, A., and Masclaux-Daubresse, C. (2005). Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis. A metabolic profiling approach 1. Plant Physiol. 138, 898-908. doi: 10.1104/pp.105.060764.898
18. Erban, A., Schauer, N., Fernie, A. R., and Kopka, J. (2007). Nonsupervised construction and application of mass spectral and retention time index libraries from time-of-flight gas chromatography-mass spectrometry metabolite profiles. Methods Mol. Biol. 358, 19-38. doi: 10.1007/978-1-59745-244-1_2
19. Fernandez, O., Béthencourt, L., Quero, A., Sangwan, R. S., and Clément Christophe, C. (2010). Trehalose and plant stress responses: friend or foe? Trends Plant Sci. 15, 409-417. doi: 10.1016/j.tplants.2010.04.004
20. Filippou, P., Antoniou, C., and Fotopoulos, V. (2013). The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic. Biol. Med. 56, 172-183. doi: 10.1016/j.freeradbiomed.2012.09.037
21. Fincato, P., Moschou, P. N., Ahou, A., Angelini, R., Roubelakis-Angelakis, K. A., Federico, R., et al. (2012). The members of Arabidopsis thaliana PAO gene family exhibit distinct tissue- and organ-specific expression pattern during seedling growth and flower development. Amino Acids 42, 831-841. doi: 10.1007/s00726-011-0999-7
22. 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
23. Fotopoulos, V., and Kanellis, A. K. (2013). Altered apoplastic ascorbate redox state in tobacco plants via ascorbate oxidase overexpression results in delayed dark-induced senescence in detached leaves. Plant Physiol. Biochem. 73, 154-160. doi: 10.1016/j.plaphy.2013.09.002
24. Foyer, C. H., and Noctor, G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 2-18. doi: 10.1104/pp.110.167569
25. Gallie, D. R. (2012). The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J. Exp. Bot. 64, 433-443. doi: 10.1093/jxb/err313
26. Gibon, Y., Pyl, E. T., Sulpice, R., Lunn, J. E., Höhne, M., Günther, M., et al. (2009). Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods.Plant Cell Environ. 32, 859-874. doi: 10.1111/j.1365-3040.2009.01965.x
27. Gibon, Y., Usadel, B., Blaesing, O. E., Kamlage, B., Hoehne, M., Trethewey, R., et al. (2006). Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol. 7:R76. doi: 10.1186/gb-2006-7-8-r76
28. Gillaspy, G. E. (2011). The cellular language of myo-Inositol signaling. New Phytol. 192, 823-839. doi: 10.1111/j.1469-8137.2011.03939.x
29. Hashida, S. N., Itami, T., Takahashi, H., Takahara, K., Nagano, M., Kawai-Yamada, M., et al. (2010). Nicotinate/nicotinamide mononucleotide adenyltransferase-mediated regulation of NAD biosynthesis protects guard cells from reactive oxygen species in ABA-mediated stomatal movement in Arabidopsis. J. Exp. Bot. 61, 3813-3825. doi: 10.1093/jxb/erq190
30. He, L., Nada, K., Kasukabe, Y., and Tachibana, S. (2002). Enhanced susceptibility of photosynthesis to low-temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of spinach (Spinacia oleracea L.). Plant Cell Physiol. 43, 196-206. doi: 10.1093/pcp/pcf021
31. Hodges, D. M., DeLong, J. M., Forney, C. F., and Prange, R. K. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604-611. doi: 10.1007/s004250050524
32. Hui, Z., Tian, F. X., Wang, G. K., Wang, G. P., and Wang, W. (2012). The antioxidative defense system is involved in the delayed senescence in a wheat mutant tasg1. Plant Cell Rep. 31, 1073-1084. doi: 10.1007/s00299-012-1226-z
33. Hummel, J., Strehmel, N., Selbig, J., Walther, D., and Kopka, J. (2010). Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics6, 322-333. doi: 10.1007/s11306-010-0198-7
34. Innocenti, G., Pucciariello, C., Le Gleuher, M., Hopkins, J., De Stefano, M., Delledonne, M., et al. (2007). Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225, 1597-1602. doi: 10.1007/s00425-006-0461-3
35. Ishizaki, K., Larson, T. R., Schauer, N., Fernie, A. R., Graham, I. A., and Leaver, C. J. (2005). The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17, 2587-2600. doi: 10.1105/tpc.105.035162
36. 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
37. Kanehisa, M., and Goto, S. (1999). KEGG: kyoto encyclopedia of genes and genomes.Nucleic Acids Res. 27, 29-34. doi: 10.1093/nar/27.1.29
38. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. (2014). Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, 199-205. doi: 10.1093/nar/gkt1076
39. Khanna-Chopra, R. (2012). Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 249, 469-481. doi: 10.1007/s00709-011-0308-z
40. Kim, D. W., Watanabe, K., Murayama, C., Izawa, S., Niitsu, M., Michael, A. J., et al. (2014). Polyamine oxidase 5 regulates Arabidopsis thaliana growth through a thermospermine oxidase activity. Plant Physiol. 168, 690-707. doi: 10.1104/pp.114.242610
41. Kopka, J., Schauer, N., Krueger, S., Birkemeyer, C., Usadel, B., Bergmüller, E., et al. (2005). GMD@CSB.DB: the golm metabolome database. Bioinformatics 21, 1635-1638. doi: 10.1093/bioinformatics/bti236
42. Krasensky, J., Broyart, C., Rabanal, F. A., and Jonak, C. (2014). The redox-sensitive chloroplast trehalose-6-phosphate phosphatase AtTPPD regulates salt stress tolerance.Antioxid. Redox Signal. 21, 1-16. doi: 10.1089/ars.2013.5693
43. Lehmann, M., Schwarzländer, M., Obata, T., Sirikantaramas, S., Burow, M., Olsen, C. E., et al. (2009). The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol. Plant 2, 390-406. doi: 10.1093/mp/ssn080
44. Linka, N., and Theodoulou, F. L. (2013). "Peroxisomes and their key role in cellular signaling and metabolism," in Peroxisomes and Their Key Role in Cellular Signaling and Metabolism, ed. R. Luis (Berlin: Springer), 169-194.
45. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A. R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc.1, 387-396. doi: 10.1038/nprot.2006.59
46. Liu, F., and Guo, F. Q. (2013). Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. PLoS ONE 8:e56345. doi: 10.1371/journal.pone.0056345
47. Liu, J. H., Kitashiba, H., Wang, J., Ban, Y., and Moriguchi, T. (2007). Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol. 24, 117-126. doi: 10.5511/plantbiotechnology.24.117
48. Liu, T., Dobashi, H., Kim, D. W., Sagor, G. H. M., Niitsu, M., Berberich, T., et al. (2014).Arabidopsis mutant plants with diverse defects in polyamine metabolism show unequal sensitivity to exogenous cadaverine probably based on their spermine content.Physiol. Mol. Biol. Plants 20, 151-159. doi: 10.1007/s12298-014-0227-5
49. López-Berges, M. S., Rispail, N., Prados-Rosales, R. C., and Di Pietro, A. (2010). A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 22, 2459-2475. doi: 10.1105/tpc.110.075937
50. Luedemann, A., Strassburg, K., Erban, A., and Kopka, J. (2008). TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 24, 732-737. doi: 10.1093/bioinformatics/btn023
51. Marcé, M., Brown, D. S., Capell, T., Figueras, X., and Tiburcio, A. F. (1995). Rapid high-performance liquid chromatographic method for the quantitation of polyamines as their dansyl derivatives: application to plant and animal tissues. J. Chromatogr. 666, 329-335. doi: 10.1016/0378-4347(94)00586-T
52. 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 Acids38, 405-413. doi: 10.1007/s00726-009-0399-4
53. Minocha, R., Majumdar, R., and Minocha, S. C. (2014). Polyamines and abiotic stress in plants: a complex relationship. Front. Plant Sci. 5:175. doi: 10.3389/fpls.2014.00175
54. Mitsuya, Y., Takahashi, Y., Berberich, T., Miyazaki, A., Matsumura, H., Takahashi, H., et al. (2009). Spermine signaling plays a significant role in the defense response ofArabidopsis thaliana to cucumber mosaic virus. J. Plant Physiol. 166, 626-643. doi: 10.1016/j.jplph.2008.08.006
55. Mohapatra, S., Minocha, R., Long, S., and Minocha, S. C. (2010). Transgenic manipulation of a single polyamine in poplar cells affects the accumulation of all amino acids. Amino Acids 38, 1117-1129. doi: 10.1007/s00726-009-0322-z
56. Molassiotis, A., and Fotopoulos, V. (2011). Oxidative and nitrosative signaling in plants: two branches in the same tree? Plant Signal. Behav. 6, 210-214. doi: 10.4161/psb.6.2.14878
57. Moschou, P. N., Paschalidis, K. A., Delis, I. D., Andriopoulou, A. H., Lagiotis, G. D., Yakoumakis, D. I., et al. (2008). 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
58. Moschou, P. N., and Roubelakis-Angelakis, K. A. (2014). Polyamines and programmed cell death. J. Exp. Bot. 65, 1285-1296. doi: 10.1093/jxb/ert373
59. 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/err313
60. Mueller, L. A., Zhang, P., and Rhee, S. Y. (2003). AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiol. 132, 453-460. doi: 10.1104/pp.102.017236
61. Navakoudis, E., Vrentzou, K., and Kotzabasis, K. (2007). A polyamine- and LHCII protease activity-based mechanism regulates the plasticity and adaptation status of the photosynthetic apparatus. Biochim. Biophys. Acta 1767, 261-271. doi: 10.1016/j.bbabio.2007.02.008
62. Niu, Y. H., and Guo, F. Q. (2012). Nitric oxide regulates dark-induced leaf senescence through EIN2 in Arabidopsis. J. Integr. Plant Biol. 54, 516-525. doi: 10.1111/j.1744-7909.2012.01140.x
63. Obata, T., Matthes, A., Koszior, S., Lehmann, M., Araújo, W. L., Bock, R., et al. (2011). Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 72, 1081-1091. doi: 10.1016/j.phytochem.2010.11.003
64. O'Hara, L. E., Paul, M. J., and Wingler, A. (2013). How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol. Plant 6, 261-274. doi: 10.1093/mp/sss120
65. Ohkama-Ohtsu, N., Oikawa, A., Zhao, P., Xiang, C., Saito, K., and Oliver, D. J. (2008). A gamma-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol. 148, 1603-1613. doi: 10.1104/pp.108.125716
66. Ohkama-Ohtsu, N., Zhao, P., Xiang, C., and Oliver, D. J. (2007). Glutathione conjugates in the vacuole are degraded by gamma-glutamyl transpeptidase GGT3 in Arabidopsis.Plant J. 49, 878-888. doi: 10.1111/j.1365-313X.2006.03005.x
67. 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
68. Pandey, S., Ranade, S. A., Nagar, P. K., and Kumar, N. (2000). Role of polyamines and ethylene as modulators of plant senescence. J. Biosci. 25, 291-299. doi: 10.1007/BF02703938
69. Paulose, B., Chhikara, S., Coomey, J., Jung, H. I., Vatamaniuk, O., and Dhankher, O. P. (2013). A γ-Glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25, 4580-4595. doi: 10.1105/tpc.113.111815
70. Piotrowski, M., Schönfelder, S., and Weiler, E. W. (2001). The Arabidopsis thalianaisogene NIT4 and its orthologs in tobacco encode β-Cyano-L-alanine Hydratase/Nitrilase. J. Biol. Chem. 276, 2616-2621. doi: 10.1074/jbc.M007890200
71. Richardson, A. D., Duigan, S. P., and Berlyn, G. P. (2002). An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytol. 153, 185-194. doi: 10.1046/j.0028-646X.2001.00289.x
72. Saeed, A. I., Sharov, V., White, J., Li, W., Liang, N., Bhagabati, J., et al. (2003). TM4: a free, open-source system for microarray data managment and analysis. BioTechniques34, 374-378.
73. Schuber, F. (1989). Influence of polyamines on membrane functions. Biochem. J. 260, 1-10. doi: 10.1042/bj2600001
74. Serafini-Fracassini, D., Di Sandro, A., and Del Duca, S. (2010). Spermine delays leaf senescence in Lactuca sativa and prevents the decay of chloroplast photosystems.Plant Physiol. Biochem. 48, 602-611. doi: 10.1016/j.plaphy.2010.03.005
75. Shelp, B. J., Bozzo, G. G., Trobacher, C. P., Zarei, A., Deyman, K. L., and Brikis, C. J. (2012). Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci. 193-194, 130-135. doi: 10.1016/j.plantsci.2012.06.001
76. Shi, H., and Chan, Z. (2014). Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J. Integr. Plant Biol. 56, 114-121. doi: 10.1111/jipb.12128
77. Sims, D. A., and Gamon, J. A. (2002). Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens. Environ. 81, 337-354. doi: 10.1016/S0034-4257(02)00010-X
78. Soudry, E., Ulitzur, S., and Gepstein, S. (2005). Accumulation and remobilization of amino acids during senescence of detached and attached leaves: in planta analysis of tryptophan levels by recombinant luminescent bacteria. J. Exp. Bot. 56, 695-702. doi: 10.1093/jxb/eri054
79. Stoynova, E. Z., Karanov, E. N., and Alexieva, V. (1999). Subcellular aspects of the protective effect of spermine against atrazine in pea plants. Plant Growth Regul. 29, 175-180. doi: 10.1023/A:1006249514986
80. Takahashi, T., and Kakehi, J.-I. (2010). Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann. Bot. 105, 1-6. doi: 10.1093/aob/mcp259
81. 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
82. Takahashi, Y., Uehara, Y., Berberich, T., Ito, A., Saitoh, H., Miyazaki, A., et al. (2004). 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
83. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., et al. (2012). Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 72, 585-599. doi: 10.1111/j.1365-313X.2012.05100.x
84. Tanou, G., Ziogas, V., Belghazi, M., Christou, A., Filippou, P., Job, D., et al. (2014). Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ. 37, 864-885. doi: 10.1111/pce.12204
85. Tavladoraki, P., Cona, A., Federico, R., Tempera, G., Viceconte, N., Saccoccio, S., et al. (2012). Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids 42, 411-426. doi: 10.1007/s00726-011-1012-1
86. Tian, F., Gong, J., Zhang, J., Zhang, M., Wang, G., Li, A., et al. (2013). Enhanced stability of thylakoid membrane proteins and antioxidant competence contribute to drought stress resistance in the tasg1 wheat stay-green mutant. J. Exp. Bot. 64, 1509-1520. doi: 10.1093/jxb/ert004
87. Tiburcio, A. F., Altabella, T., Bitrián, M., and Alcázar, R. (2014). The roles of polyamines during the lifespan of plants: from development to stress. Planta 240, 1-18. doi: 10.1007/s00425-014-2055-9
88. Tisi, A., Angelini, R., and Cona, A. (2011). Does polyamine catabolism influence root development and xylem differentiation under stress conditions? Plant Signal. Behav. 6, 1844-1847. doi: 10.4161/psb.6.11.17640
89. Tripathi, D. N., Chowdhury, R., Trudel, L. J., Tee, A. R., Slack, R. S., Walker, C. L., et al. (2013). Reactive nitrogen species regulate autophagy through ATM-AMPK-TSC2-mediated suppression of mTORC1. Proc. Natl. Acad. Sci. U.S.A. 110:E2950. doi: 10.1073/pnas.1307736110
90. Van der Graaff, E., Schwacke, R., Schneider, A., Desimone, M., and Kunze, R. (2006). Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 141, 776-792. doi: 10.1104/pp.106.079293.Leaf
91. Van Houtte, H., Vandesteene, L., López-Galvis, L., Lemmens, L., Kissel, E., Carpentier, S., et al. (2013). Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in abscisic acid-induced stomatal closure. Plant Physiol. 161, 1158-1171. doi: 10.1104/pp.112.211391
92. Velikova, V., Yordanov, I., and Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci. 151, 59-66. doi: 10.1016/S0168-9452(99)00197-1
93. Wang, W., Vignani, R., Scali, M., and Cresti, M. (2006). A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis.Electrophoresis 27, 2782-2786. doi: 10.1002/elps.200500722
94. Wang, Z., Xiao, Y., Chen, W., Tang, K., and Zhang, L. (2010). Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J. Integr. Plant Biol. 52, 400-409. doi: 10.1111/j.1744-7909.2010.00921.x
95. Watanabe, M., Balazadeh, S., Tohge, T., Erban, A., Giavalisco, P., Kopka, J., et al. (2013). Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol.162, 1290-1310. doi: 10.1104/pp.113.217380
96. Williams, S. P., Gillaspy, G. E., and Perera, I. Y. (2015). Biosynthesis and possible functions of inositol pyrophosphates in plants. Front. Plant Sci. 6:67. doi: 10.3389/fpls.2015.00067
97. Yaakoubi, H., Hamdani, S., Bekalé, L., and Carpentier, R. (2014). Protective action of spermine and spermidine against photoinhibition of photosystem i in isolated thylakoid membranes. PLoS ONE 9:e112893. doi: 10.1371/journal.pone.0112893
98. Yamagami, T., Tsuchisaka, A., Yamada, K., Haddon, W. F., Harden, L. A., and Theologis, A. (2003). Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J. Biol. Chem. 278, 49102-49112. doi: 10.1074/jbc.M308297200
99. Zhao, Y. (2014). Auxin Biosynthesis. Arab. B. 12:e0173. doi: 10.1199/tab.0173
100. Zhou, B., Guo, Z., Xing, J., and Huang, B. (2005). Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J. Exp. Bot. 56, 3223-3228. doi: 10.1093/jxb/eri319