Identification of a drimenol synthase and drimenol oxidase from Persicaria hydropiper, involved in the biosynthesis of insect deterrent drimanes

Plant J. 2017 Jun;90(6):1052-1063. doi: 10.1111/tpj.13527. Epub 2017 Apr 26.

Abstract

The sesquiterpenoid polygodial, which belongs to the drimane family, has been shown to be an antifeedant for a number of herbivorous insects. It is presumed to be synthesized from farnesyl diphosphate via drimenol, subsequent C-12 hydroxylation and further oxidations at both C-11 and C-12 to form a dialdehyde. Here, we have identified a drimenol synthase (PhDS) and a cytochrome P450 drimenol oxidase (PhDOX1) from Persicaria hydropiper. Expression of PhDS in yeast and plants resulted in production of drimenol alone. Co-expression of PhDS with PhDOX1 in yeast yielded drimendiol, the 12-hydroxylation product of drimenol, as a major product, and cinnamolide. When PhDS and PhDOX1 were transiently expressed by agro-infiltration in Nicotiana benthamiana leaves, drimenol was almost completely converted into cinnamolide and several additional drimenol derivatives were observed. In vitro assays showed that PhDOX1 only catalyses the conversion from drimenol to drimendiol, and not the further oxidation into an aldehyde. In yeast and heterologous plant hosts, the C-12 position of drimendiol is therefore likely to be further oxidized by endogenous enzymes into an aldehyde and subsequently converted to cinnamolide, presumably by spontaneous hemiacetal formation with the C-11 hydroxyl group followed by oxidation. Purified cinnamolide was confirmed by NMR and shown to be deterrent with an effective deterrent dose (ED50 ) of about 200-400 μg g-1 fresh weight against both whiteflies and aphids. The putative additional physiological and biochemical requirements for polygodial biosynthesis and stable storage in plant tissues are discussed.

Keywords: Persicaria hydropiper; CYP76AJ1; cinnamolide; drimane sequiterpenes; drimendiol; drimenol; insect deterrent.

MeSH terms

  • Animals
  • Aphids / drug effects
  • Hemiptera / drug effects
  • Nicotiana / enzymology
  • Nicotiana / genetics
  • Nicotiana / metabolism
  • Plant Extracts / metabolism
  • Plant Extracts / pharmacology
  • Plant Leaves / enzymology
  • Plant Leaves / genetics
  • Plant Leaves / metabolism
  • Plants, Genetically Modified / enzymology
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • Polycyclic Sesquiterpenes
  • Polygonaceae / enzymology*
  • Polygonaceae / genetics
  • Polygonaceae / metabolism*
  • Sesquiterpenes / metabolism*
  • Sesquiterpenes / pharmacology
  • Terpenes / metabolism

Substances

  • Plant Extracts
  • Polycyclic Sesquiterpenes
  • Sesquiterpenes
  • Terpenes
  • drimane
  • drimenol

Associated data

  • GENBANK/KC754968
  • GENBANK/KC754969