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Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana

Plant Cell Reports volume 29, pages 955–965 (2010)Cite this article

Abstract

The genome of Arabidopsis thaliana contains five genes (AtPAO1 to AtPAO5) encoding polyamine oxidase (PAO) which is an enzyme responsible for polyamine catabolism. To understand the individual roles of the five AtPAOs, here we characterized their tissue-specific and space-temporal expression. AtPAO1 seems to have a specific function in flower organ. AtPAO2 was expressed in shoot meristem and root tip of seedlings, and to a higher extent in the later growth stage within restricted parts of the organs, such as shoot meristem, leaf petiole and also in anther. The expression of AtPAO3 was constitutive, but highest in flower organ. AtPAO3 promoter activity was detected in cotyledon, distal portion of root, boundary region of mature rosette leaf and in filaments of flower. AtPAO4 was expressed at higher level all over young seedlings including roots, and in the mature stage its expression was ubiquitous with rather lower level in stem. AtPAO5 expression was observed in the whole plant body throughout various growth stages. Its highest expression was in flowers, particularly in sepals, but not in petals. Furthermore, we determined the substrate specificity of AtPAO1 to AtPAO4. None of the AtPAO enzymes recognized putrescine (Put). AtPAO2 and AtPAO3 showed almost similar substrate recognition patterns in which the most preferable substrate is spermidine (Spd) followed by less specificity to other tetraamines tested. AtPAO4 seemed to be spermine (Spm)-specific. More interestingly, AtPAO1 preferred thermospermine (T-Spm) and norspermine (NorSpm) to Spm, but did not recognize Spd. Based on the results, the individual function of AtPAOs is discussed.

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Abbreviations

AO:

Amine oxidase

NorSpm:

Norspermine

N1-AcSpm:

N1-Acetylspermine

PAO:

Polyamine oxidase

PCR:

Polymerase chain reaction

Put:

Putrescine

Spd:

Spermidine

Spm:

Spermine

T-Spm:

Thermospermine

References

  • Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876

    Article  PubMed  Google Scholar 

  • Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317

    Article  CAS  PubMed  Google Scholar 

  • Binda C, Coda A, Angelini R, Federico R, Ascenzi P, Mattevi A (1999) A 30-Å-long U-shaped catalytic tunnel in the crystal structure of polyamine oxidase. Structure 7:265–276

    Article  CAS  PubMed  Google Scholar 

  • Bolenius FN, Seiler N (1981) Acetyl derivatives as intermediates in polyamine catabolism. Int J Biochem 13:287–292

    Article  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin TJ (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Cervelli M, Tavladoraki 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 38:667–677

    Article  CAS  Google Scholar 

  • Cervelli 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 268:3816–3830

    Article  CAS  PubMed  Google Scholar 

  • Cervelli M, Polticelli F, Federico R, Mariottini P (2003) Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 278:5271–5276

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Cohen SS (1998) A guide to the polyamines. Oxford University Press, Oxford

    Google Scholar 

  • Cona A, Moreno S, Cenci F, Federico R, Angelini R (2005) Cellular redistribution of flavin-containing polyamine oxidase in differentiating root and mesocotyl of Zea mays L. seedlings. Planta 221:265–276

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Del Duca S, Beninati S, Serafini-Fracassini D (1995) Polyamines in chloroplasts: identification of their glutamyl and acetyl derivatives. Biochem J 305:233–237

    CAS  PubMed  Google Scholar 

  • Federico R, Angelini R (1991) Polyamine catabolism in plants. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton, pp 41–56

    Google Scholar 

  • Fuell C, Elliot KA, Hanfrey CC, Franceschetti M, Michael AJ (2010) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem (in press)

  • Groppa MD, Benavides MP (2007) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  • Kakehi J, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Knott JM, Romer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086

    Article  CAS  PubMed  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  PubMed  Google Scholar 

  • Lim TS, Chitra TR, Han P, Pua EC, Yu H (2006) Cloning and characterization of Arabidopsis and Brassica juncea flavin-containing amine oxidases. J Exp Bot 57:4155–4169

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Naka Y, Watanabe K, Sagor G.H.M, Niitsu M, Pillai A, Kusano T, Takahashi Y (2010) Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiol Biochem (in press)

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233

    CAS  PubMed  Google Scholar 

  • Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99

    CAS  PubMed  Google Scholar 

  • Tassoni A, Van Buuren M, Franceschetti M, Fornale IS, Bagni N (2000) Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. Plant Physiol Biochem 38:383–393

    Article  CAS  Google Scholar 

  • Tavladoraki P, Shinina 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 426:62–66

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14

    Article  CAS  PubMed  Google Scholar 

  • Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wu T, Yankovskaya V, McIntire WS (2003) Cloning, sequencing, and heterologous expression of the murine peroxisomal flavoprotein, N 1-acetylated polyamine oxidase. J Biol Chem 278:20514–20525

    Article  CAS  PubMed  Google Scholar 

  • 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 142:193–206

    Article  CAS  PubMed  Google Scholar 

  • Yoda Y, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxidein host- and nonhost hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by Grant-in-Aids from the Japan Society for the Promotion of Science (JSPS) to TK (21380063) and YT (21780087). TB was supported by a JSPS-BRIDGE fellowship (BR090101).

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Authors and Affiliations

  1. Laboratory of Plant Molecular and Cellular Biology, Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba, Sendai, Miyagi, 980-8577, Japan

    Yoshihiro Takahashi, Runzi Cong, G. H. M. Sagor, Thomas Berberich & Tomonobu Kusano

  2. Faculty of Pharmaceutical Sciences, Josai University, Sakado, Saitama, 370-0290, Japan

    Masaru Niitsu

  3. Biodiversity and Climate Research Center Frankfurt, Frankfurt, Germany

    Thomas Berberich

Authors
  1. Yoshihiro Takahashi
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  2. Runzi Cong
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  3. G. H. M. Sagor
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  4. Masaru Niitsu
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  5. Thomas Berberich
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  6. Tomonobu Kusano
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Corresponding authors

Correspondence to Yoshihiro Takahashi or Tomonobu Kusano.

Additional information

Communicated by H. Ebinuma.

Y. Takahashi and R. Cong contributed equally to this work.

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Takahashi, Y., Cong, R., Sagor, G.H.M. et al. Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana . Plant Cell Rep 29, 955–965 (2010). https://doi.org/10.1007/s00299-010-0881-1

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  • DOI: https://doi.org/10.1007/s00299-010-0881-1

Keywords

  • A. thaliana
  • Gene expression
  • Polyamine oxidase
  • Space-temporal expression
  • Substrate specificity