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.

Genes Involved in Stress Response and Especially in Phytoalexin Biosynthesis Are Upregulated in Four Malus Genotypes in Response to Apple Replant Disease

“…The putative mannosidase gene MNL2 belongs to the glucose-methanol-choline oxidoreductase family. Genes of this family are involved in adaptive processes in plant-insect interactions during host-dependent chemical defense (Rahfeld et al, 2014). However, the detailed function of the MNL2 gene in plants is still unknown.…”

Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

“…Following uptake of the glycoside into the glandular reservoirs by a highly specific transport system, a b-glucosidase of glycoside hydrolase family 1 releases 8-hydroxygeraniol, which is then oxidized to 8-oxogeranial. Notably, this oxidation step is catalyzed by a flavoprotein oxidoreductase of the glucose-methanol-choline (GMC) superfamily, which is different from the 8-hydroxygeraniol oxidoreductase used by plants (Rahfeld et al, 2014(Rahfeld et al, , 2015 Fig. 4).…”

Natural Varroa mite-surviving Apis mellifera honeybee populations

“…A promising candidate gene identified in this genomic region of the honeybee that may be significant in affecting the mite's reproduction was a glucosemethanol-choline oxidoreductase (GMCOX18). Oxidoreductase genes have been reported to be involved in diverse functions for A. mellifera including cuticle biosynthesis (Kunieda et al 2006) and are involved in larval chemical defenses in other insects, such as leaf beetles, by displaying a glandular secretion that repels enemies (Chrysomelidae ; Michalski et al 2008;Rahfeld et al 2014). This candidate gene could be involved in altered brood volatiles that influence mite oogenesis, which would support earlier hypotheses for the mechanisms behind the reduced mite reproductive success in the population.…”