Polyamine oxidase5 regulates arabidopsis growth through thermospermine oxidase activity

Dong Wook Kim, Kanako Watanabe, Chihiro Murayama, Sho Izawa, Masaru Niitsu, Anthony J. Michael, Thomas Berberich, Tomonobu Kusano

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

The major plant polyamines (PAs) are the tetraamines spermine (Spm) and thermospermine (T-Spm), the triamine spermidine, and the diamine putrescine. PA homeostasis is governed by the balance between biosynthesis and catabolism; the latter is catalyzed by polyamine oxidase (PAO). Arabidopsis (Arabidopsis thaliana) has five PAO genes, AtPAO1 to AtPAO5, and all encoded proteins have been biochemically characterized. All AtPAO enzymes function in the back-conversion of tetraamine to triamine and/or triamine to diamine, albeit with different PA specificities. Here, we demonstrate that AtPAO5 loss-of-function mutants (pao5) contain 2-fold higher T-Spm levels and exhibit delayed transition from vegetative to reproductive growth compared with that of wild-type plants. Although the wild type and pao5 are indistinguishable at the early seedling stage, externally supplied low-dose T-Spm, but not other PAs, inhibits aerial growth of pao5 mutants in a dose-dependent manner. Introduction of wild-type AtPAO5 into pao5 mutants rescues growth and reduces the T-Spm content, demonstrating that AtPAO5 is a T-Spm oxidase. Recombinant AtPAO5 catalyzes the conversion of T-Spm and Spm to triamine spermidine in vitro. AtPAO5 specificity for T-Spm in planta may be explained by coexpression with T-Spm synthase but not with Spm synthase. The pao5 mutant lacking T-Spm oxidation and the acl5 mutant lacking T-Spm synthesis both exhibit growth defects. This study indicates a crucial role for T-Spm in plant growth and development.

Original languageEnglish (US)
Pages (from-to)1575-1590
Number of pages16
JournalPlant Physiology
Volume165
Issue number4
DOIs
StatePublished - 2014

Fingerprint

Polyamines
polyamines
Arabidopsis
Oxidoreductases
mutants
Growth
diamines
spermine
spermidine
Diamines
Spermidine
Spermine
putrescine
dosage
Plantae
Spermine Synthase
plant development
thermospermine
homeostasis
growth and development

ASJC Scopus subject areas

  • Plant Science
  • Genetics
  • Physiology

Cite this

Kim, D. W., Watanabe, K., Murayama, C., Izawa, S., Niitsu, M., Michael, A. J., ... Kusano, T. (2014). Polyamine oxidase5 regulates arabidopsis growth through thermospermine oxidase activity. Plant Physiology, 165(4), 1575-1590. https://doi.org/10.1104/pp.114.242610

Polyamine oxidase5 regulates arabidopsis growth through thermospermine oxidase activity. / Kim, Dong Wook; Watanabe, Kanako; Murayama, Chihiro; Izawa, Sho; Niitsu, Masaru; Michael, Anthony J.; Berberich, Thomas; Kusano, Tomonobu.

In: Plant Physiology, Vol. 165, No. 4, 2014, p. 1575-1590.

Research output: Contribution to journalArticle

Kim, DW, Watanabe, K, Murayama, C, Izawa, S, Niitsu, M, Michael, AJ, Berberich, T & Kusano, T 2014, 'Polyamine oxidase5 regulates arabidopsis growth through thermospermine oxidase activity', Plant Physiology, vol. 165, no. 4, pp. 1575-1590. https://doi.org/10.1104/pp.114.242610
Kim, Dong Wook ; Watanabe, Kanako ; Murayama, Chihiro ; Izawa, Sho ; Niitsu, Masaru ; Michael, Anthony J. ; Berberich, Thomas ; Kusano, Tomonobu. / Polyamine oxidase5 regulates arabidopsis growth through thermospermine oxidase activity. In: Plant Physiology. 2014 ; Vol. 165, No. 4. pp. 1575-1590.
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