title: Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana.
abstract: BACKGROUND
  Polyamines (PAs) are oxidatively deaminated at their primary or secondary amino-groups by copper-containing amine oxidases (CuAOs) or FAD-dependent amine oxidases (PAOs), respectively. Both enzymes have long been considered to be apoplastic proteins. However, three out of five PAO isoforms in Arabidopsis thaliana are localized in peroxisomes, while the other two PAOs are predicted to be cytosolic. Interestingly, most of these PAOs do not contribute to terminal PA oxidation, but instead are involved in the back-conversion pathway, producing spermidine from spermine and putrescine from spermidine, which in turn is inhibited by putrescine. This opens the question as to whether PAs are catabolized in the apoplast of Arabidopsis and if the terminal oxidation occurs in the peroxisomes. The main objective of this study was to know if these catabolic processes are mediated by CuAOs.
  
  
  RESULTS
  A. thaliana contains ten genes annotated as CuAOs, but only one (ATAO1) has been characterized at the protein level. Reported herein is the characterization of three genes encoding putative Arabidopsis CuAOs (AtCuAO1, AtCuAO2 and AtCuAO3). These genes encode functional CuAOs that use putrescine and spermidine as substrates. AtCuAO1, like ATAO1, is an extracellular protein, while AtCuAO2 and AtCuAO3 are localized in peroxisomes. The three genes present a different expression profile in response to exogenous treatments, such as application of abcisic acid, methyl jasmonate, salycilic acid, flagellin 22 and wounding.
  
  
  CONCLUSIONS
  PA catabolism in the Arabidopsis apoplast is mediated predominantly by CuAOs, while in peroxisomes the co-localization of CuAO-dependent terminal catabolism with PAO-back-conversion machineries might contribute to modulating putrescine-mediated inhibition of the back-conversion, suggesting the occurrence of a tight coordination between both catabolic pathways. The expression profile of AtCuAO1-3 in response to different exogenous treatments, together with the different localization of the corresponding proteins, provides evidence for the functional diversification of Arabidopsis CuAO proteins.
authors.affiliation: Department of Molecular Genetics, Centre for Research in Agricultural Genomics (CSIC-IRTA-UAB-UB), Campus UAB, Bellaterra (Cerdanyola del Vallès), Barcelona, Spain.
authors.forename: Joan
authors.initials: J
authors.lastname: Planas-Portell
authors.forename: Marta
authors.initials: M
authors.lastname: Gallart
authors.forename: Antonio F
authors.initials: AF
authors.lastname: Tiburcio
authors.forename: Teresa
authors.initials: T
authors.lastname: Altabella
mesh_terms: D006631:Amine Oxidase (Copper-Containing) / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000737:chemistry / Q000201:enzymology* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D005110:Extracellular Space / Q000201:enzymology / Q000235:genetics; D015971:Gene Expression Regulation, Enzymologic; D008969:Molecular Sequence Data; D010084:Oxidation-Reduction; D020675:Peroxisomes / Q000737:chemistry / Q000201:enzymology* / Q000235:genetics; D011073:Polyamines / Q000378:metabolism*; D021381:Protein Transport; D016415:Sequence Alignment
chemical_list: D029681:Arabidopsis Proteins; D011073:Polyamines; D006631:Amine Oxidase (Copper-Containing)
references.citation: Structure. 1996 Aug 15;4(8):943-55
references.pmid: 8805580
references.citation: Plant Physiol. 2009 Apr;149(4):1970-81
references.pmid: 19218362
references.citation: Plant Physiol. 2009 May;150(1):125-43
references.pmid: 19329564
references.citation: Phytochemistry. 2003 Sep;64(1):97-107
references.pmid: 12946408
references.citation: Plant Physiol. 2006 Sep;142(1):193-206
references.pmid: 16844838
references.citation: J Gen Virol. 2006 Nov;87(Pt 11):3413-3423
references.pmid: 17030878
references.citation: Methods Mol Biol. 2009;483:193-208
references.pmid: 19183900
references.citation: Trends Plant Sci. 2012 May;17(5):260-70
references.pmid: 22498450
references.citation: J Biol Chem. 1992 Apr 25;267(12):7979-82
references.pmid: 1569055
references.citation: Mol Plant. 2011 Jul;4(4):663-78
references.pmid: 21471330
references.citation: Plant Cell Physiol. 2008 Sep;49(9):1272-82
references.pmid: 18703589
references.citation: Biochemistry. 1992 Dec 8;31(48):12147-54
references.pmid: 1457410
references.citation: Amino Acids. 2012 Feb;42(2-3):411-26
references.pmid: 21874532
references.citation: Plant Signal Behav. 2008 Dec;3(12):1061-6
references.pmid: 19513239
references.citation: Plant J. 2007 Sep;51(6):1126-36
references.pmid: 17666025
references.citation: Plant J. 2005 Mar;41(5):767-78
references.pmid: 15703063
references.citation: J Biol Chem. 1995 Jul 14;270(28):16939-46
references.pmid: 7622512
references.citation: Plant Physiol. 2008 Dec;148(4):1809-29
references.pmid: 18931141
references.citation: Plant J. 2005 Aug;43(3):425-36
references.pmid: 16045477
references.citation: Plant Physiol. 2008 Oct;148(2):1094-105
references.pmid: 18701673
references.citation: Plant Physiol. 2006 Aug;141(4):1519-32
references.pmid: 16778015
references.citation: Plant Signal Behav. 2008 Mar;3(3):204-6
references.pmid: 19704660
references.citation: Planta. 2011 Feb;233(2):369-82
references.pmid: 21053011
references.citation: J Inorg Biochem. 2007 Jul;101(7):997-1004
references.pmid: 17521737
references.citation: Plant Physiol. 2008 Aug;147(4):1845-57
references.pmid: 18583528
references.citation: Plant Cell Rep. 2010 Sep;29(9):955-65
references.pmid: 20532512
references.citation: Plant J. 2006 Feb;45(4):616-29
references.pmid: 16441352
references.citation: Biochim Biophys Acta. 2000 Jul 14;1480(1-2):329-41
references.pmid: 11004571
references.citation: Nucleic Acids Res. 2007 Jan;35(Database issue):D213-8
references.pmid: 17071959
references.citation: Biochemistry. 1997 Feb 18;36(7):1608-20
references.pmid: 9048544
references.citation: Planta. 2008 Aug;228(3):367-81
references.pmid: 18594857
references.citation: Plant Physiol. 2004 Sep;136(1):2621-32
references.pmid: 15375207
references.citation: Comput Appl Biosci. 1994 Feb;10(1):19-29
references.pmid: 8193951
references.citation: Amino Acids. 2004 Dec;27(3-4):347-58
references.pmid: 15592759
references.citation: Structure. 1995 Nov 15;3(11):1171-84
references.pmid: 8591028
references.citation: Plant Physiol. 2002 Mar;128(3):865-75
references.pmid: 11891243
references.citation: Plant Physiol. 2004 Apr;134(4):1414-26
references.pmid: 15064377
references.citation: Plant Cell. 2008 Jun;20(6):1708-24
references.pmid: 18577660
references.citation: FEBS Lett. 1999 Jun 18;453(1-2):1-5
references.pmid: 10403363
references.citation: J Plant Physiol. 2007 Nov;164(11):1410-8
references.pmid: 17728013
references.citation: Plant Physiol Biochem. 2010 Jul;48(7):560-4
references.pmid: 20219383
references.citation: Plant J. 1998 Jan;13(2):153-65
references.pmid: 9680973
references.citation: J Exp Bot. 2011 Jan;62(3):1155-68
references.pmid: 21081665
references.citation: Plant Physiol. 2005 Aug;138(4):2174-84
references.pmid: 16040649
references.citation: Amino Acids. 2004 Jun;26(3):217-33
references.pmid: 15221502
references.citation: Plant Physiol. 2008 Aug;147(4):2164-78
references.pmid: 18583531
references.citation: Planta. 2010 May;231(6):1237-49
references.pmid: 20221631
references.citation: Trends Plant Sci. 2006 Feb;11(2):80-8
references.pmid: 16406305
references.citation: Plant J. 1998 Mar;13(6):781-91
references.pmid: 9681017