ALLENE OXIDE CYCLASE (AOC) gene family members of Arabidopsis thaliana: tissue- and organ-specific promoter activities and in vivo heteromerization

J Exp Bot. 2012 Oct;63(17):6125-38. doi: 10.1093/jxb/ers261. Epub 2012 Oct 1.

Abstract

Jasmonates are important signals in plant stress responses and plant development. An essential step in the biosynthesis of jasmonic acid (JA) is catalysed by ALLENE OXIDE CYCLASE (AOC) which establishes the naturally occurring enantiomeric structure of jasmonates. In Arabidopsis thaliana, four genes encode four functional AOC polypeptides (AOC1, AOC2, AOC3, and AOC4) raising the question of functional redundancy or diversification. Analysis of transcript accumulation revealed an organ-specific expression pattern, whereas detailed inspection of transgenic lines expressing the GUS reporter gene under the control of individual AOC promoters showed partially redundant promoter activities during development: (i) In fully developed leaves, promoter activities of AOC1, AOC2, and AOC3 appeared throughout all leaf tissue, but AOC4 promoter activity was vascular bundle-specific; (ii) only AOC3 and AOC4 showed promoter activities in roots; and (iii) partially specific promoter activities were found for AOC1 and AOC4 in flower development. In situ hybridization of flower stalks confirmed the GUS activity data. Characterization of single and double AOC loss-of-function mutants further corroborates the hypothesis of functional redundancies among individual AOCs due to a lack of phenotypes indicative of JA deficiency (e.g. male sterility). To elucidate whether redundant AOC expression might contribute to regulation on AOC activity level, protein interaction studies using bimolecular fluorescence complementation (BiFC) were performed and showed that all AOCs can interact among each other. The data suggest a putative regulatory mechanism of temporal and spatial fine-tuning in JA formation by differential expression and via possible heteromerization of the four AOCs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / cytology
  • Arabidopsis / drug effects
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Cyclopentanes / metabolism*
  • Dimerization
  • Flowers / cytology
  • Flowers / drug effects
  • Flowers / enzymology
  • Flowers / genetics
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Plant
  • Genes, Reporter
  • Intramolecular Oxidoreductases / genetics*
  • Intramolecular Oxidoreductases / metabolism
  • Multigene Family
  • Mutation
  • Nicotiana / genetics
  • Nicotiana / metabolism
  • Organ Specificity
  • Oxylipins / metabolism*
  • Plant Leaves / cytology
  • Plant Leaves / drug effects
  • Plant Leaves / enzymology
  • Plant Leaves / genetics
  • Plant Roots / cytology
  • Plant Roots / drug effects
  • Plant Roots / enzymology
  • Plant Roots / genetics
  • Plant Vascular Bundle / cytology
  • Plant Vascular Bundle / drug effects
  • Plant Vascular Bundle / enzymology
  • Plant Vascular Bundle / genetics
  • Plants, Genetically Modified
  • Promoter Regions, Genetic / genetics
  • Protein Interaction Mapping
  • RNA, Messenger / genetics
  • RNA, Plant / genetics
  • Seeds / cytology
  • Seeds / drug effects
  • Seeds / enzymology
  • Seeds / genetics

Substances

  • Arabidopsis Proteins
  • Cyclopentanes
  • Oxylipins
  • RNA, Messenger
  • RNA, Plant
  • jasmonic acid
  • Intramolecular Oxidoreductases
  • AOC2 protein, Arabidopsis
  • hydroperoxide isomerase