Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles: MOLECULAR AND FUNCTIONAL CHARACTERIZATION OF TWO NEW MEMBERS OF THE GLUCOSE-METHANOL-CHOLINE OXIDOREDUCTASE GENE FAMILY

Carmen Michalski,Hoda Mohagheghi,Manfred Nimtz,Jacques Pasteels,Dietrich Ober

doi:10.1074/jbc.m802236200

Abstract

Salicyl alcohol oxidase is an extracellular enzyme that occurs in glandular reservoirs of chrysomelid leaf beetle larvae and catalyzes the formation of salicylaldehyde, a volatile deterrent used by the larvae against predators. Salicyl alcohol is the hydrolysis product of salicin, a plant-derived precursor taken up by the beetle larvae from the leaves of willow and poplar trees. The cDNA encoding salicyl alcohol oxidase from two related species Chrysomela tremulae and Chrysomela populi has been identified, cloned, and expressed in an active form in Escherichia coli. The open reading frame of 623 amino acids begins in both enzymes with an N-terminal signal peptide of 21 amino acids. Sequence comparison has revealed that salicyl alcohol oxidase belongs to the family of glucose-methanol-choline oxidoreductase-like sequences with mostly unknown function. Enzymes of this family share similar overall structure with an essentially identical FAD-binding site but possess different catalytic activities. The data suggest that salicyl alcohol oxidase, essential for the activation of the plant-derived precursor salicin, was originally recruited from an oxidase involved in the autogenous biosynthesis of iridoid monoterpenes and found in related chrysomelid leaf beetle species.

Highlights

Chrysomelid leaf beetles encompass a taxon of about 40,000 mainly phytophagous species [1]
Salicyl alcohol oxidase is an extracellular enzyme that occurs in glandular reservoirs of chrysomelid leaf beetle larvae and catalyzes the formation of salicylaldehyde, a volatile deterrent used by the larvae against predators
The data suggest that salicyl alcohol oxidase, essential for the activation of the plant-derived precursor salicin, was originally recruited from an oxidase involved in the autogenous biosynthesis of iridoid monoterpenes and found in related chrysomelid leaf beetle species

Summary

Introduction

Chrysomelid leaf beetles encompass a taxon of about 40,000 mainly phytophagous species [1]. Phylogenetic analyses have shown that the de novo synthesis of iridoid monoterpenes is the most ancestral type of chemical defense, of which the host-derived salicylaldehyde strategy has evolved at least twice during the evolution of the Chrysomeline leaf beetles. This strategy has itself been replaced in some of the more recent lineages by mixed metabolism involving the synthesis of butyric acids [11].

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