The protein quality control system manages plant defence compound synthesis

Nature. 2013 Dec 5;504(7478):148-52. doi: 10.1038/nature12685. Epub 2013 Nov 10.

Abstract

Jasmonates are ubiquitous oxylipin-derived phytohormones that are essential in the regulation of many development, growth and defence processes. Across the plant kingdom, jasmonates act as elicitors of the production of bioactive secondary metabolites that serve in defence against attackers. Knowledge of the conserved jasmonate perception and early signalling machineries is increasing, but the downstream mechanisms that regulate defence metabolism remain largely unknown. Here we show that, in the legume Medicago truncatula, jasmonate recruits the endoplasmic-reticulum-associated degradation (ERAD) quality control system to manage the production of triterpene saponins, widespread bioactive compounds that share a biogenic origin with sterols. An ERAD-type RING membrane-anchor E3 ubiquitin ligase is co-expressed with saponin synthesis enzymes to control the activity of 3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), the rate-limiting enzyme in the supply of the ubiquitous terpene precursor isopentenyl diphosphate. Thus, unrestrained bioactive saponin accumulation is prevented and plant development and integrity secured. This control apparatus is equivalent to the ERAD system that regulates sterol synthesis in yeasts and mammals but that uses distinct E3 ubiquitin ligases, of the HMGR degradation 1 (HRD1) type, to direct destruction of HMGR. Hence, the general principles for the management of sterol and triterpene saponin biosynthesis are conserved across eukaryotes but can be controlled by divergent regulatory cues.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Endoplasmic Reticulum-Associated Degradation
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant*
  • Gene Silencing
  • Genetic Complementation Test
  • Medicago truncatula / enzymology
  • Medicago truncatula / genetics*
  • Medicago truncatula / metabolism*
  • Medicago truncatula / ultrastructure
  • Microscopy, Electron, Scanning
  • Molecular Sequence Data
  • Mutation
  • Plant Growth Regulators / metabolism
  • Plant Roots / genetics
  • Plant Roots / metabolism
  • Plant Roots / ultrastructure
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism
  • Saponins / biosynthesis
  • Saponins / genetics
  • Signal Transduction
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Plant Growth Regulators
  • Saponins
  • Ubiquitin-Protein Ligases

Associated data

  • GENBANK/JF714982