title: Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve.
abstract: Larvae of the leaf beetle subtribe Chrysomelina sensu stricto repel their enemies by displaying glandular secretions that contain defensive compounds. These repellents can be produced either de novo (iridoids) or by using plant-derived precursors (e.g. salicylaldehyde). The autonomous production of iridoids, as in Phaedon cochleariae, is the ancestral chrysomeline chemical defence and predates the evolution of salicylaldehyde-based defence. Both biosynthesis strategies include an oxidative step of an alcohol intermediate. In salicylaldehyde-producing species, this step is catalysed by salicyl alcohol oxidases (SAOs) of the glucose-methanol-choline (GMC) oxidoreductase superfamily, but the enzyme oxidizing the iridoid precursor is unknown. Here, we show by in vitro as well as in vivo experiments that P. cochleariae also uses an oxidase from the GMC superfamily for defensive purposes. However, our phylogenetic analysis of chrysomeline GMC oxidoreductases revealed that the oxidase of the iridoid pathway originated from a GMC clade different from that of the SAOs. Thus, the evolution of a host-independent chemical defence followed by a shift to a host-dependent chemical defence in chrysomeline beetles coincided with the utilization of genes from different GMC subfamilies. These findings illustrate the importance of the GMC multi-gene family for adaptive processes in plant-insect interactions.
authors.affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Peter
authors.initials: P
authors.lastname: Rahfeld
authors.affiliation: Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Roy
authors.initials: R
authors.lastname: Kirsch
authors.affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Susann
authors.initials: S
authors.lastname: Kugel
authors.affiliation: Research Group Mass Spectrometry/Proteomics, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Natalie
authors.initials: N
authors.lastname: Wielsch
authors.affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Stock
authors.affiliation: Genome Analysis Group, Leibniz Institute for Age Research, Fritz Lipmann Institute, Jena, Germany.
authors.forename: Marco
authors.initials: M
authors.lastname: Groth
authors.affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Wilhelm
authors.initials: W
authors.lastname: Boland
authors.affiliation: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany aburse@ice.mpg.de.
authors.forename: Antje
authors.initials: A
authors.lastname: Burse
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D001517:Coleoptera / Q000201:enzymology / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D007814:Larva / Q000201:enzymology / Q000235:genetics / Q000378:metabolism; D008969:Molecular Sequence Data; D009928:Organ Specificity; D010088:Oxidoreductases / Q000235:genetics* / Q000378:metabolism; D010802:Phylogeny; D016415:Sequence Alignment
chemical_list: D019476:Insect Proteins; D010088:Oxidoreductases
keywords: RNA interference; chemical defence; insects; iridoid biosynthesis; phylogeny; secretions