Glandular β-glucosidases in juvenile Chrysomelina leaf beetles support the evolution of a host-plant-dependent chemical defense

• Published in: Insect biochemistry and molecular biology 2015-03, Vol.58, p.28-38
• Main Authors: Rahfeld, Peter, Haeger, Wiebke, Kirsch, Roy, Pauls, Gerhard, Becker, Tobias, Schulze, Eva, Wielsch, Natalie, Wang, Ding, Groth, Marco, Brandt, Wolfgang, Boland, Wilhelm, Burse, Antje
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Animals; Biological Evolution; Cellulases - biosynthesis; Cellulases - metabolism; Chrysomelidae; Coleoptera - enzymology; Coleoptera - growth & development; Coleoptera - metabolism; Enzyme kinetics; Evolution; Homology modeling; Insect; Iridoids - metabolism; Larva - enzymology; Larva - metabolism; Molecular Sequence Data; Phylogeny; Plant Leaves - chemistry; Plant Leaves - parasitology; Plants - chemistry; Plants - parasitology; RNA Interference; β-Glucosidase
• ISSN: 0965-1748; 1879-0240
• DOI: 10.1016/j.ibmb.2015.01.003

Plant-feeding insects are spread across the entire plant kingdom. Because they chew externally on leaves, leaf beetle of the subtribe Chrysomelina sensu stricto are constantly exposed to life-threatening predators and parasitoids. To counter these pressures, the juveniles 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. The autonomous production of iridoids pre-dates the evolution of phytochemical-based defense strategies. Both strategies include hydrolysis of the secreted non-toxic glycosides in the defensive exudates. By combining in vitro as well as in vivo experiments, we show that iridoid de novo producing as well as sequestering species rely on secreted β-glucosidases to cleave the pre-toxins. Our phylogenetic analyses support a common origin of chrysomeline β-glucosidases. The kinetic parameters of these β-glucosidases demonstrated substrate selectivity which reflects the adaptation of Chrysomelina sensu stricto to the chemistry of their hosts during the course of evolution. However, the functional studies also showed that the broad substrate selectivity allows building a chemical defense, which is dependent on the host plant, but does not lead to an “evolutionary dead end”. [Display omitted] •Three glandular-specific β-glucosidases have been identified from phylogenetically related leaf beetle species.•RNA interference showed importance of the β-glucosidases for the production of defensive secretions in vivo.•Purified β-glucosidases demonstrated broad selectivity with preference for their respective physiological substrate.•Enzymatic properties of β-glucosidases can contribute to the evolutionary dynamics of host-plant affiliation in beetles.