Polyamine oxidase5 regulates arabidopsis growth through thermospermine oxidase activity

Plant Physiology

Volumn 165, Issue 4, 2014, Pages 1575-1590

  Kim, Dong Wook ^a   Watanabe, Kanako ^a   Murayama, Chihiro ^a   Izawa, Sho ^a   Niitsu, Masaru ^b   Michael, Anthony J ^c   Berberich, Thomas ^d   Kusano, Tomonobu ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b JOSAI UNIVERSITY   (Japan)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84905223925     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.242610     Document Type: Article

References (60)

1. Ahou A, Martignago D, Alabdallah O, Tavazza R, Stano P, Macone A, Pivato M, Masi A, Rambla JL, Vera-Sirera F, et al (2014) A plant spermine oxidase/dehydrogenase regulated by the proteasome and polyamines. J Exp Bot 65: 1585-1603
2. Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231: 1237-1249
3. Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P, Tisi A (2010) Plant amine oxidases "on the move": an update. Plant Physiol Biochem 48: 560-564
4. Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, Cona A (2008) Involvement of polyamine oxidase in wound healing. Plant Physiol 146: 162-177
5. Benítez M, Hejátko J (2013) Dynamics of cell-fate determination and patterning in the vascular bundles of Arabidopsis thaliana. PLoS ONE 8: e63108
6. Bonke M, Thitamadee S, Mähönen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426: 181-186
7. Cervelli M, Polticelli F, Federico R, Mariottini P (2003) Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 278: 5271-5276
8. Chen J, Acton TB, Basu SK, Montelione GT, Inouye M (2002) Enhancement of the solubility of proteins overexpressed in Escherichia coli by heat shock. J Mol Microbiol Biotechnol 4: 519-524
9. Clay NK, Nelson T (2005) Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cellspecific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138: 767-777
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11: 80-88
12. Cui X, Ge C, Wang R, Wang H, Chen W, Fu Z, Jiang X, Li J, Wang Y (2010) The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis. Cell Res20: 576-586
13. Fincato P, Moschou PN, Ahou A, Angelini R, Roubelakis-Angelakis KA, Federico R, Tavladoraki P (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
14. Fincato P, Moschou PN, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis KA, Tavladoraki P (2011) Functional diversity inside the Arabidopsis polyamine oxidase gene family. J Exp Bot 62: 1155-1168
15. Fuse T, Sasaki T, Yano M (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol 18: 219-222
16. Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16: 446-456
17. Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J 27: 551-560
18. Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19: 4248-4256
19. Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, et al (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135: 1565-1573
20. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5: 387-405
21. Kakehi J, Kuwashiro Y, Motose H, Igarashi K, Takahashi T (2010) Norspermine substitutes for thermospermine in the control of stem elongation in Arabidopsis thaliana. FEBS Lett 584: 3042-3046
22. Kakehi J, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49: 1342-1349
23. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49: 1272-1282
24. Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581: 3081-3086
25. Koizumi K, Yokoyama R, Nishitani K (2009) Mechanical load induces upregulation of transcripts for a set of genes implicated in secondary wall formation in the supporting tissue of Arabidopsis thaliana. J Plant Res 122: 651-659
26. Kumar A, Taylor MA, Arif SAM, Davies HV (1996) Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) trans-genes show altered levels of polyamines and ethylene: Antisense plants display abnormal phenotypes. Plant J 9: 147-158
27. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228: 367-381
28. Ling Q, Huang W, Jarvis P (2011) Use of a SPAD-502 meter to measure leaf chlorophyll concentration in Arabidopsis thaliana. Photosynth Res 107: 209-214
29. Liu T, Kim DW, Niitsu M, Berberich T, Kusano T (2014a) Oryza sativa polyamine oxidase 1 back-converts tetraamines, spermine and thermospermine, to spermidine. Plant Cell Rep 33: 143-151
30. Liu T, Kim DW, Niitsu M, Maeda S, Watanabe S, Kamio Y, Berberich T, Kusano T (2014b) Polyamine oxidase 7 is a terminal catabolism-type enzyme in Oryza sativa and is specifically expressed in anthers. Plant Cell Physiol 55: 1110-1122
31. Mattoo AK, Minocha SC, Minocha R, Handa AK (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
32. Milhinhos A, Prestele J, Bollhöner B, Matos A, Vera-Sirera F, Rambla JL, Ljung K, Carbonell J, Blázquez MA, Tuominen H, et al (2013) Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem. Plant J 75: 685-698
33. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008) 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
34. Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau Courtois CL, Carbonell J, Blázquez MA, Tuominen H (2008) ACAU-LIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135: 2573-2582
35. Naka Y, Watanabe K, Sagor GHM, Niitsu M, Pillai MA, Kusano T, Takahashi Y (2010) Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiol Biochem 48: 527-533
36. Niitsu M, Samejima K (1986) Synthesis of a series of linear pentaamines with three and four methylene chain intervals. Chem Pharm Bull (Tokyo) 34: 1032-1038
37. Ono Y, Kim DW, Watanabe K, Sasaki A, Niitsu M, Berberich T, Kusano T, Takahashi Y (2012) Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino Acids 42: 867-876
38. Panicot M, Minguet EG, Ferrando A, Alcázar R, Blázquez MA, Carbonell J, Altabella T, Koncz C, Tiburcio AF (2002) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14: 2539-2551
39. Sagor GHM, Yamaguchi K, Watanabe K, Berberich T, Kusano T, Takahashi Y (2011) Spatio-temporal expression analysis of Arabidopsis thaliana spermine synthase gene promoter. Plant Biotechnol 28: 407-411
40. Samejima K, Takeda Y, Kawase M, Okada M, Kyogoku Y (1984) Syntheses of 15N-enriched polyamines. Chem Pharm Bull (Tokyo) 32: 3428-3435
41. Takahashi T, Kakehi J (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot (Lond) 105: 1-6
42. Takahashi Y, Cong R, Sagor GHM, Niitsu M, Berberich T, Kusano T (2010) Characterization of five polyamine oxidase isoforms in Arabi-dopsis thaliana. Plant Cell Rep 29: 955-965
43. Takano A, Kakehi J, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53: 606-616
44. Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Federico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141: 1519-1532
45. Tavladoraki P, Schininà ME, Cecconi F, Di Agostino S, Manera F, Rea G, Mariottini P, Federico R, Angelini R (1998) Maize polyamine oxidase: primary structure from protein and cDNA sequencing. FEBS Lett 426:60-62
46. Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139: 1840-1852
47. Tiburcio AF, Altabella T, Bitrián M, Alczar R (March 23, 2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 228: 367-381 http://dx.doi.org/10.1007/s00425-014-2055-9
48. Tisi A, Federico R, Moreno S, Lucretti S, Moschou PN, Roubelakis-Angelakis KA, Angelini R, Cona A (2011) Perturbation of polyamine catabolism can strongly affect root development and xylem differentiation. Plant Physiol 157: 200-215
49. Tong W, Yoshimoto K, Kakehi J, Motose H, Niitsu M, Takahashi T (2014) Thermospermine modulates expression of auxin-related genes in Arabidopsis. Front Plant Sci 5: 94
50. Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579: 1557-1564
51. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blázquez MA, Carbonell J (2010) Role of polyamines in plant vascular development. Plant Physiol Biochem 48: 534-539
52. Vujcic S, Diegelman P, Bacchi CJ, Kramer DL, Porter CW (2002) Identification and characterization of a novel flavin-containing spermine oxidase of mammalian cell origin. Biochem J 367: 665-675
53. Vujcic S, Liang P, Diegelman P, Kramer DL, Porter CW (2003) Genomic identification and biochemical characterization of the mammalian polyamine oxidase involved in polyamine back-conversion. Biochem J 370: 19-28
54. Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376: 1-14
55. Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA Jr (2001) Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 61: 5370-5373
56. Wang Y, Murray-Stewart T, Devereux W, Hacker A, Frydman B, Woster PM, Casero RA Jr (2003) Properties of purified recombinant human polyamine oxidase, PAOh1/SMO. Biochem Biophys Res Commun 304: 605-611
57. Wu T, Yankovskaya V, McIntire WS (2003) Cloning, sequencing, and heterologous expression of the murine peroxisomal flavoprotein, N1-acetylated polyamine oxidase. J Biol Chem 278: 20514-20525
58. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
59. Yoshimoto K, Noutoshi Y, Hayashi K, Shirasu K, Takahashi T, Motose H (2012) A chemical biology approach reveals an opposite action between thermospermine and auxin in xylem development in Arabidopsis thaliana. Plant Cell Physiol 53: 635-645
60. Zhu XJ, Thalor SK, Takahashi Y, Berberich T, Kusano T (2012) An inhibitory effect of the sequence-conserved upstream open reading frame on the translation of the main open-reading frame of HsfB1 transcripts in Arabidopsis. Plant Cell Environ 35: 2014-2030