Advertisement

Journal of Plant Research

, Volume 131, Issue 2, pp 341–348 | Cite as

Highly-expressed polyamine oxidases catalyze polyamine back conversion in Brachypodium distachyon

  • Yoshihiro Takahashi
  • Kaede Ono
  • Yuuta Akamine
  • Takuya Asano
  • Masatoshi Ezaki
  • Itsupei Mouri
Regular Paper
  • 140 Downloads

Abstract

To understand the polyamine (PA) catabolic pathways in Brachypodium distachyon, we focused on the flavin-containing polyamine oxidase enzymes (PAO), and characterized them at the molecular and biochemical levels. Five PAO isoforms were identified from database searches, and we named them BdPAO1 to BdPAO5. By gene expression analysis using above-ground tissues such as leaf, stem and inflorescence, it was revealed that BdPAO2 is the most abundant PAO gene in normal growth conditions, followed by BdPAO3 and BdPAO4. BdPAO1 and BdPAO5 were expressed at very low levels. All Arabidopsis thaliana and rice orthologs belonging to the same clade as BdPAO2, BdPAO3 and BdPAO4 have conserved peroxisome-targeting signal sequences at their C-termini. Amino acid sequences of BdPAO2 and BdPAO4 also showed such a sequence, but BdPAO3 did not. We selected the gene with the highest expression level (BdPAO2) and the peroxisome-targeting signal lacking PAO (BdPAO3) for biochemical analysis of substrate specificity and catabolic pathways. BdPAO2 catalyzed conversion of spermine (Spm) or thermospermine to spermidine (Spd), and Spd to putrescine, but its most-favored substrate was Spd. In contrast, BdPAO3 favored Spm as substrate and catalyzed conversion of tetraamines to Spd. These results indicated that the major PAOs in B. distachyon have back-conversion activity.

Keywords

Back-conversion Brachypodium distachyon Peroxisome-targeting signal Polyamine oxidase Spermidine Spermine 

Notes

Acknowledgements

We thank RIKEN BRC for providing B. distachyon Bd21 seeds. This study was supported in part by a Grant-in-Aid from the Japan Society for the Promotion of Science, to YT (16K07607). We thank James Allen, DPhil, from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

Supplementary material

10265_2017_989_MOESM1_ESM.pdf (221 kb)
Supplementary material 1 (PDF 220 KB)

References

  1. Agostinelli E, Condello M, Molinari A, Tempera G, Viceconte N, Arancia G (2009) Cytotoxicity of spermine oxidation products to multidrug resistant melanoma M14 ADR2 cells: sensitization by MDL 72527 lysosomotropic compound. Int J Oncol 35:485–498CrossRefPubMedGoogle Scholar
  2. Ahou A, Martignago D, Alabdallah O, Tavazza R, Stano P, Macone A, Pivato M, Masi A, Rambla JL, Vera-Sirera F, Angelini R, Federico R, Tavladoraki P (2014) A plant spermine oxidase/dehydrogenase regulated by the proteasome and polyamines. J Exp Bot 65:1585–1603CrossRefPubMedGoogle Scholar
  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 48:560–564CrossRefPubMedGoogle Scholar
  4. Averill-Bates DA, Ke Q, Tanel A, Roy J, Fortier G, Agostinelli E (2008) Mechanism of vell death induced by spermine and amine oxidase in mouse melanoma cells. Int J Oncol 32:79–88PubMedGoogle Scholar
  5. Bevan MW, Garvin DF, Vogel JP (2010) Brachypodium distachyon genomics for sustainable food and fuel production. Curr Opin Biotech 21:211–217CrossRefPubMedGoogle Scholar
  6. Carvelli M, Cona A, Angelini R, Polticelli F, Federico R, Mariottini P (2001) A barley polyamine oxidase isoform with distinct structural features and subcellular localization. Eur J Biochem 268:3816–3830CrossRefGoogle Scholar
  7. Cervelli M, Tavladorali P, Di Agostino S, Angelini R, Federico R, Mariottini P (2000) Isolation and characterization of three polyamine oxidase genes from Zea mays. Plant Physiol Biochem 38:667–677CrossRefGoogle Scholar
  8. Cervelli M, Di Caro O, Di Penta A, Angellini R, Federico R, Vitale A, Mariottini P (2004) A novel C-terminal sequence from barley polyamine oxidase is a vacuolar sorting signal. Plant J 40:410–418CrossRefPubMedGoogle Scholar
  9. Cervelli M, Bianchi M, Cona A, Crosatti C, Stanca M, Angelini R, Federico R, Mariottini P (2006) Barley polyamine oxidase isoforms 1 and 2, a peculiar case of gene duplication. FEBS J 273:3990–4002CrossRefPubMedGoogle Scholar
  10. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88CrossRefPubMedGoogle Scholar
  11. Federico R, Con A, Angelini R, Schininà ME, Giartosio A (1990) Characterization of maize polyamine oxidase. Phytochemistry 29:2411–2414CrossRefPubMedGoogle Scholar
  12. Federico R, Ercolini L, Laurenzi M, Angelini R (1996) Oxidation of acetylpolyamines by maize amine oxidase gene family. Phytochemistry 43:339–341CrossRefGoogle Scholar
  13. 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 62:1155–1168CrossRefPubMedGoogle Scholar
  14. Hamana K, Matsuzaki S (1985) Distinct difference in the polyamine compositions of Bryophyta and Pteridophyta. J Biochem 97:1595–1601CrossRefPubMedGoogle Scholar
  15. Hong S-Y, Seo PJ, Yang M-S, Xiang F, Park C-M (2008) Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR. BMC Plant Biol 8:112. doi: 10.1186/1471-2229-/8/112 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotech Adv 29:300–311CrossRefGoogle Scholar
  17. 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 49:1272–1282CrossRefPubMedGoogle Scholar
  18. Koc EC, Bagga S, Songstad DD, Betz SR, Kuehn GD, Phillips GC (1998) Occurrence of uncommon polyamines in cultured tissues of maize. In Vitro Cell Dev Biol-Plant 34:252–255CrossRefGoogle Scholar
  19. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350CrossRefPubMedGoogle Scholar
  20. Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381CrossRefPubMedGoogle Scholar
  21. Liu T, Kim DW, Niitsu M, Maeda S, Watanabe M, Kamio Y, Berberich T, Kusano T (2014) Polyamine oxidase 7 is a terminal catabolism-type enzyme in Oryza sativa and is specifically expressed in anthers. Plant Cell Physiol 55:1110–1122CrossRefPubMedGoogle Scholar
  22. Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008a) 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 147:1845–1857CrossRefPubMedPubMedCentralGoogle Scholar
  23. Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008b) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 48:527–533CrossRefPubMedGoogle Scholar
  25. 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 42:867–876CrossRefPubMedGoogle Scholar
  26. Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109CrossRefPubMedPubMedCentralGoogle Scholar
  27. Radová A, Šebela M, Galuszka P, Frébort I, Jacobsen S, Faulhammer HG, Peč P (2001) Barley polyamine oxidase: characterization and analysis of the cofactor and the N-terminal amino acid sequence. Phytochem Anal 12:166–173CrossRefPubMedGoogle Scholar
  28. Rambla JL, Vera-Sirera F, Blázquez MA, Carbonell J, Granell A (2010) Quantitation of biogenic tetraamines in Arabidopsis thaliana. Analytic Biochem 397:208–211CrossRefGoogle Scholar
  29. Reumann S (2004) Specification of the peroxidase targeting signals type1 and type2 of plant peroxisomes by bioinformatics analyses. Plant physiol 135:783–800CrossRefPubMedPubMedCentralGoogle Scholar
  30. Rodríguez AA, Maiale SJ, Menéndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262CrossRefPubMedGoogle Scholar
  31. Rodriguez-Garay B, Phillips GC, Kuehn GD (1989) Detection of norspermidine and norspermine in Medicago sativa L. (alfalfa). Plant Physiol 89:525–529CrossRefPubMedPubMedCentralGoogle Scholar
  32. Šebela M, Radová A, Angelini R, Tavladoraki P, Frébort I, Peč P (2001) FAD-containing polyamine oxidases: a timely challenge for researcher in biochemistry and physiology of plants. Plant Sci 160:197–207CrossRefPubMedGoogle Scholar
  33. Sharmin S, Sakata K, Kashiwagi K, Ueda S, Iwasaki S, Shirahata A, Igarashi K (2001) Polyamine cytotoxicity in the presence of bovine serum amine oxidase. Biochem Biophys Res Commun 282:228–235CrossRefPubMedGoogle Scholar
  34. Takahashi Y (2016) The role of polyamines in plant disease resistance. Environ Control Biol 54:17–21CrossRefGoogle Scholar
  35. Takahashi Y, Cong R, Sagor GHM, Miitsu M, Berberich T, Kusano T (2010) Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep 29:955–965CrossRefPubMedGoogle Scholar
  36. Takano A, Kakehi J-I, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53:606–616CrossRefPubMedGoogle Scholar
  37. 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 426:62–66CrossRefPubMedGoogle Scholar
  38. 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 141:1519–1532CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tavladoraki P, Cona A, Federico R, Tempera G, Viceconte N, Saccoccio S, Battaglia V, Toninello A, Agostinelli E (2012) Polyamine catabolism: target for antiproliferative therapies in animals and stress tolerance strategies in plants. Amino Acids 42:411–426CrossRefPubMedGoogle Scholar
  40. 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 157:200–215CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wu J, Shang Z, Wu J, Jiang X, Moschou PN, Sun W, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63:1042–1053CrossRefPubMedGoogle Scholar
  42. Yoda H, Hiroi Y, 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 142:193–206CrossRefPubMedPubMedCentralGoogle Scholar
  43. Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxide in host- and nonhost hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  • Yoshihiro Takahashi
    • 1
  • Kaede Ono
    • 1
  • Yuuta Akamine
    • 1
  • Takuya Asano
    • 1
  • Masatoshi Ezaki
    • 1
  • Itsupei Mouri
    • 1
  1. 1.Department of Applied Chemistry and Biochemistry, Faculty of EngineeringKyushu Sangyo UniversityFukuokaJapan

Personalised recommendations