Molecular evolution of N-methylputrescine oxidase in tobacco

Plant Cell Physiol. 2014 Feb;55(2):436-44. doi: 10.1093/pcp/pct179. Epub 2013 Nov 28.

Abstract

Biosynthesis of nicotine in tobacco requires N-methylputrescine oxidase (MPO), which belongs to the copper-containing amine oxidase superfamily. Previous studies identified tobacco MPO1 and its close homolog NtDAO1 (formerly called MPO2), of which MPO1 has been shown preferentially to oxidize N-methylated amines. We show here that NtDAO1, as well as a homologous Arabidopsis diamine oxidase (DAO), accept non-N-methylated amines more efficiently than their corresponding N-methylated amines. MPO1 is coordinately regulated with other nicotine biosynthesis genes with regard to COI1-MYC2-dependent jasmonate induction and its dependence on nicotine-specific ERF transcription factors, whereas NtDAO1 is constitutively expressed at low basal levels in tobacco plants. Both MPO1 and NtDAO1 are targeted to peroxisomes by their C-terminal motifs, and the peroxisomal localization of MPO1 is required for it to function in nicotine biosynthesis in jasmonate-elicited cultured tobacco cells. Restricted occurrence of the MPO subfamily in Nicotiana and Solanum indicates that, during the formation of the Solanaceae, MPO has evolved from a DAO, which functions in polyamine catabolism within peroxisomes, by optimizing substrate preference and gene expression patterns to be suitable for alkaloid formation.

Keywords: Diamine oxidase; Nicotine; Peroxisomes; Putrescine; Tobacco.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaloids / analysis
  • Alkaloids / metabolism
  • Amine Oxidase (Copper-Containing) / genetics*
  • Amine Oxidase (Copper-Containing) / metabolism
  • Arabidopsis / cytology
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Cyclopentanes / metabolism
  • Evolution, Molecular
  • Gene Expression Regulation, Plant*
  • Models, Biological
  • Nicotiana / cytology
  • Nicotiana / enzymology*
  • Nicotiana / genetics
  • Nicotine / metabolism
  • Oxylipins / metabolism
  • Peroxisomes / metabolism
  • Plant Growth Regulators / metabolism
  • Plant Leaves / cytology
  • Plant Leaves / enzymology
  • Plant Leaves / genetics
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Roots / cytology
  • Plant Roots / enzymology
  • Plant Roots / genetics
  • Plants, Genetically Modified
  • Promoter Regions, Genetic
  • Protein Transport
  • Putrescine / metabolism*
  • RNA Interference
  • Recombinant Proteins
  • Substrate Specificity

Substances

  • Alkaloids
  • Cyclopentanes
  • Oxylipins
  • Plant Growth Regulators
  • Plant Proteins
  • Recombinant Proteins
  • Nicotine
  • jasmonic acid
  • Amine Oxidase (Copper-Containing)
  • Putrescine