Molecular cloning and functional characterization of psoralen synthase, the first committed monooxygenase of furanocoumarin biosynthesis

J Biol Chem. 2007 Jan 5;282(1):542-54. doi: 10.1074/jbc.M604762200. Epub 2006 Oct 26.

Abstract

Ammi majus L. accumulates linear furanocoumarins by cytochrome P450 (CYP)-dependent conversion of 6-prenylumbelliferone via (+)-marmesin to psoralen. Relevant activities, i.e. psoralen synthase, are induced rapidly from negligible background levels upon elicitation of A. majus cultures with transient maxima at 9-10 h and were recovered in labile microsomes. Expressed sequence tags were cloned from elicited Ammi cells by a nested DD-RT-PCR strategy with CYP-specific primers, and full-size cDNAs were generated from those fragments correlated in abundance with the induction profile of furanocoumarin-specific activities. One of these cDNAs representing a transcript of maximal abundance at 4 h of elicitation was assigned CYP71AJ1. Functional expression in Escherichia coli or yeast cells initially failed but was accomplished eventually in yeast cells after swapping the N-terminal membrane anchor domain with that of CYP73A1. The recombinant enzyme was identified as psoralen synthase with narrow substrate specificity for (+)-marmesin. Psoralen synthase catalyzes a unique carbon-chain cleavage reaction concomitantly releasing acetone by syn-elimination. Related plants, i.e. Heracleum mantegazzianum, are known to produce both linear and angular furanocoumarins by analogous conversion of 8-prenylumbelliferone via (+)-columbianetin to angelicin, and it was suggested that angelicin synthase has evolved from psoralen synthase. However, (+)-columbianetin failed as substrate but competitively inhibited psoralen synthase activity. Analogy modeling and docked solutions defined the conditions for high affinity substrate binding and predicted the minimal requirements to accommodate (+)-columbianetin in the active site cavity. The studies suggested that several point mutations are necessary to pave the road toward angelicin synthase evolution.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Ammi / enzymology*
  • Binding Sites
  • Cloning, Molecular
  • Cytochrome P-450 Enzyme System / chemistry*
  • Escherichia coli / metabolism
  • Furocoumarins / biosynthesis*
  • Mass Spectrometry
  • Mixed Function Oxygenases / chemistry*
  • Models, Molecular
  • Molecular Sequence Data
  • Plant Proteins / chemistry
  • Sequence Homology, Amino Acid
  • Substrate Specificity
  • Umbelliferones / chemistry

Substances

  • Furocoumarins
  • Plant Proteins
  • Umbelliferones
  • 7-hydroxycoumarin
  • Cytochrome P-450 Enzyme System
  • Mixed Function Oxygenases
  • psoralen synthase