Abstract
Key message
Oryza sativa polyamine oxidase 1 back-converts spermine (or thermospermine) to spermidine. Considering the previous work, major path of polyamine catabolism in rice plant is suggestive to be back-conversion but not terminal catabolism.
Abstract
Rice (Oryza sativa) contains seven genes encoding polyamine oxidases (PAOs), termed OsPAO1 to OsPAO7, based on their chromosomal number and gene ID number. We previously showed that three of these members, OsPAO3, OsPAO4 and OsPAO5, are abundantly expressed, that their products localize to peroxisomes and that they catalyze the polyamine back-conversion reaction. Here, we have focused on OsPAO1. The OsPAO1 gene product shares a high level of identity with those of Arabidopsis PAO5 and Brassica juncea PAO. Expression of OsPAO1 appears to be quite low under physiological conditions, but is markedly induced in rice roots by spermine (Spm) or T-Spm treatment. Consistent with the above finding, the recombinant OsPAO1 prefers T-Spm as a substrate at pH 6.0 and Spm at pH 8.5 and, in both cases, back-converts these tetraamines to spermidine, but not to putrescine. OsPAO1 localizes to the cytoplasm of onion epidermal cells. Differing in subcellular localization, four out of seven rice PAOs, OsPAO1, OsPAO3, OsPAO4 and OsPAO5, catalyze back-conversion reactions of PAs. Based on the results, we discuss the catabolic path(s) of PAs in rice plant.
Similar content being viewed by others
References
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
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
Casero RA Jr, Pegg AE (1993) Spermidine/spermine N1-acetyltransferase—the turning point in polyamine metabolism. FASEB J 7:653–661
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
Cervelli M, Polticelli F, Federico R, Mariottini P (2003) Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 278:5271–5276
Cervelli M, Caro OD, Penta AD, Angelini R, Federico R, Vitale A, Mariottini P (2004) A novel C-terminal sequence from barley polyamine oxidase is a vacuolar sorting signal. Plant J 40:410–418
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 273:3990–4002
Chen J, Acton TB, Basu SK, Montelion GT, Inoue M (2002) Enhancement of the solubility of proteins overexpressed in Escherichia coli by heat shock. J Mol Microbiol Biotechnol 4:519–524
Cohen SS (1998) A guide to the polyamines. Oxford University Press, Oxford
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
Federico R, Cona A, Angelini R, Schininà ME, Giartosio A (1990) Characterization of maize polyamine oxidase. Phytochemistry 29:2411–2414
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
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
Fuse T, Sasaki T, Yano M (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol 18:219–222
Handa AK, Mattoo AK (2010) Differential and functional interactions emphasize the multiple roles of polyamines in plants. Plant Physiol Biochem 48:540–546
Hood EE, Helmer GL, Fraley RT, Chilton MD (1986) The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J Bacteriol 168:1291–1301
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
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
Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings Bioinform 9:299–306
Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381
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
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
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
Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015
Naka Y, Watanabe K, Sagor GHM, Niitsu M, Pillai A, Kusano T, Takahashi Y (2010) Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiol Biochem 48:527–533
Niitsu M, Samejima K (1986) Syntheses of a series of linear pentaamines with three and four methylene chain intervals. Chem Pharm Bull 34:1032–1038
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 catalyzed polyamine back conversion. Amino Acids 42:867–876
Samejima K, Takeda M, Kawase M, Okada M, Kyogoku Y (1984) Syntheses of 15N-enriched polyamines. Chem Pharm Bull 32:3428–3435
Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790
Takahashi Y, Cong R, Sagor GHM, Niitsu M, Berberich T, Kusano T (2010) Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep 29:955–965
Takano A, Kakehi JI, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53:606–616
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
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
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976
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
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
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
Acknowledgments
We gratefully acknowledge Drs. M. Yano, M. Teranishi and J. Hidema for providing plasmids and bacterial strains. This study was supported by the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) to TK (21380063) and to DWK (25·5682, Grant-in-Aid for Young Scientists) and grants from The Saito Gratitude Foundation and The Japan Science Society (The Sasagawa Scientific Research Grant) to DWK. TL was financially supported by the China Scholarship Council.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Ebinuma.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, T., Kim, D.W., Niitsu, M. et al. Oryza sativa polyamine oxidase 1 back-converts tetraamines, spermine and thermospermine, to spermidine. Plant Cell Rep 33, 143–151 (2014). https://doi.org/10.1007/s00299-013-1518-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-013-1518-y