Biosynthesis of iridoid monoterpenes in insects: Defensive secretions from larvae of leaf beetles (coleoptera: chrysomelidae).

Veith, Martin; Lorenz, Michael; Boland, Wilhelm; Simon, Helmut; Dettner, Konrad

doi:10.1016/s0040-4020(01)81338-7

Cited by 52 publications

(59 citation statements)

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“…Phylogenetic analyses of Chrysomelina sensu stricto species revealed that the composition of their secretions reflects a stepwise scenario of host -plant adaptation [5]. The evolutionary history of the larval chemical defence started with the de novo production of deterrent iridoids (cyclopentanoid monoterpenoids) that does not rely on the secondary metabolites of their hosts [14,15]. Derived from this autonomous biosynthesis, two lineages independently developed a defensive strategy that relies on the sequestration of salicin (figure 1), a plant-derived precursor from Salicaceae used to produce the deterrent salicylaldehyde [5].…”

Section: Introductionmentioning

confidence: 99%

Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve

et al. 2014

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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.

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Section: Introductionmentioning

confidence: 99%

Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve

et al. 2014

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“…Most leaf beetle species are highly specialized on a single plant genus, where they spend their whole life cycle. Their well-defended larvae exhibit different degrees of dependence on the host plant's secondary metabolites (9)(10)(11)(12)(13).…”

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Host plant shifts affect a major defense enzyme inChrysomela lapponica

Kirsch

Vogel

Muck

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Chrysomelid leaf beetles use chemical defenses to overcome predatory attack and microbial infestation. Larvae of Chrysomela lapponica that feed on willow sequester plant-derived salicin and other leaf alcohol glucosides, which are modified in their defensive glands to bioactive compounds. Salicin is converted into salicylaldehyde by a consecutive action of a β-glucosidase and salicyl alcohol oxidase (SAO). The other leaf alcohol glucosides are not oxidized, but are deglucosylated and esterified with isobutyricand 2-methylbutyric acid. Like some other closely related Chrysomela species, certain populations of C. lapponica shift host plants from willow to salicin-free birch. The only striking difference between willow feeders and birch feeders in terms of chemical defense is the lack of salicylaldehyde formation. To clarify the impact of host plant shifts on SAO activity, we identified and compared this enzyme by cloning, expression, and functional testing in a willow-feeding and birch-feeding population of C. lapponica. Although the birch feeders still demonstrated defensive glandspecific expression, their SAO mRNA levels were 1,000-fold lower, and the SAO enzyme was nonfunctional. Obviously, the loss of catalytic function of the SAO of birch-adapted larvae is fixed at the transcriptional, translational, and enzyme levels, thus avoiding costly expression of a highly abundant protein that is not required in the birch feeders.host plant adaptation | glucose-methanol-choline oxidoreductase M ost phytophagous insects are specialized to a restricted set of host plant species (1-4). Host affiliation/specialization has been shown to be influenced by geographical, genetic, biophysical, and ecological enforcements (3, 5). But the most important barriers are toxic metabolites of the host plant (6-8), which all phytophagous insects must overcome by developing appropriate detoxification mechanisms. Adapting to plant-specific chemicals provides insects with a niche that allows them to survive, but narrows the range within which host plant shifts can occur, including only plants with similar metabolite patterns.Chrysomelina leaf beetles are an excellent taxon for investigating host plant adaptation and relevant factors associated with host plant shifts. Most leaf beetle species are highly specialized on a single plant genus, where they spend their whole life cycle. Their well-defended larvae exhibit different degrees of dependence on the host plant's secondary metabolites (9-13).

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“…Each gland consists of several gland cells that are attached to a glandular reservoir whose content is everted when the larvae is disturbed. The defensive secretions of larvae belonging to the subtribe Chrysomelina have been analyzed, and three strategies have been identified that reflect different degrees of specialization during evolution: first, the de novo production of iridoid monoterpenes from terpenoid precursors, providing an autogenous defense that is completely host plant-independent (7,8); second, the biosynthesis of the aromatic compound salicylaldehyde from salicin, a phenolic glucoside taken up from the larval host plant, in a strategy that is fully dependent upon the chemistry of the host plant (9); third, the biosynthesis of esters composed of de novo-synthesized butyric acids with the alcohol moiety of leaf alcohol glucosides retrieved from the plant, representing a strategy partially dependent on the chemistry of the host plant (10).…”

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“…Pasteels et al (4) have postulated that the enzymes involved in the biosynthesis of salicylaldehyde might have evolved from enzymes catalyzing the final steps in the production of iridoid monoterpenes. As a precursor of iridoid monoterpenes, 8-hydroxygeraniol-8-O-␤-D-glucoside is synthesized in the glands from geraniol via 8-hydroxygeraniol (7,15,16) before it is secreted into the glandular reservoir. In the reservoir, the glycoside is cleaved by an extracellular ␤-glucosidase, and the aglycon is subsequently oxidized, yielding the dialdehyde 8-oxocitral.…”

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Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles

Michalski

Mohagheghi

Nimtz

et al. 2008

Journal of Biological Chemistry

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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.

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Biosynthesis of iridoid monoterpenes in insects: Defensive secretions from larvae of leaf beetles (coleoptera: chrysomelidae).

Cited by 52 publications

References 25 publications

Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve

Independently recruited oxidases from the glucose-methanol-choline oxidoreductase family enabled chemical defences in leaf beetle larvae (subtribe Chrysomelina) to evolve

Host plant shifts affect a major defense enzyme inChrysomela lapponica

Salicyl Alcohol Oxidase of the Chemical Defense Secretion of Two Chrysomelid Leaf Beetles

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