Biosynthesis of Defensive Allomones in Leaf Beetle Larvae: Stereochemistry of Salicylalcohol Oxidation in Phratora vitellinae and Comparison of Enzyme Substrate and Stereospecificity with Alcohol Oxidases from Several Iridoid Producing Leaf Beetles

Veith, Martin; Oldham, Neil J.; Dettner, Konrad; Pasteels, Jacques; Boland, Wilhelm

doi:10.1023/b:joec.0000006369.26490.c6

Cited by 23 publications

(26 citation statements)

References 13 publications

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“…Phratora vitellinae is a salicin-sequestering species which is evolutionarily isolated within the iridoid producers without having a close relationship to the salicylaldehyde-producing genus Chrysomela (figure 1). Substrate tests with secretions revealed the oxidation of both salicyl alcohol and the precursor for iridoids, 8-hydroxygeraniol [20,27]. However, the activity of the recently identified Ph.…”

Section: Discussionmentioning

confidence: 99%

“…Early biochemical investigations of secretions in iridoid-(Phaedon amoraciae, Phratora laticollis) and salicylaldehyde-(Phratora vitellinae) producing species revealed side activities for the non-natural substrates salicyl alcohol and 8-hydroxygeraniol, respectively [27]. These results suggest a change in the specificity of the oxidase over the course of Chrysomelina sensu stricto evolution [5,20].…”

Section: Introductionmentioning

confidence: 99%

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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: Discussionmentioning

confidence: 99%

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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“…This process is facilitated also by the observation that the first enzymes in the reservoirs (glucosidases) are generally unspecific. Subsequent adaptation of the more selective oxidases (16,32) is likely to occur and does not require enzymatic ''innovations.'' The highest evolved leaf beetles (e.g., Chrysomela interrupta, see Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Because the basal species and the more advanced sequestering species share not only the principal architecture of their defensive system but also several enzymatic activities (see Fig. 1), the shift from de novo to host-derived defense may require only small changes in the specificity of enzymes present in the glands and reservoir (11,16). Certainly, also the ability to acquire ''unfamiliar'' plant metabolites from food plays a pivotal role because the import system is the first molecular mechanism that selects for appropriate molecules that are delivered to the glandular system.…”

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confidence: 99%

Selective transport systems mediate sequestration of plant glucosides in leaf beetles: A molecular basis for adaptation and evolution

Kuhn

Pettersson

Feld

et al. 2004

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

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Chrysomeline larvae respond to disturbance and attack by everting dorsal glandular reservoirs, which release defensive secretions. The ancestral defense is based on the de novo synthesis of monoterpene iridoids. The catabolization of the host-plant O-glucoside salicin into salicylaldehyde is a character state that evolved later in two distinct lineages, which specialized on Salicaceae. By using two species producing monoterpenes (Hydrothassa marginella and Phratora laticollis) and two sequestering species (Chrysomela populi and Phratora vitellinae), we studied the molecular basis of sequestration by feeding the larvae structurally different thioglucosides resembling natural O-glucosides. Their accumulation in the defensive systems demonstrated that the larvae possess transport systems, which are evolutionarily adapted to the glycosides of their host plants. Minor structural modifications in the aglycon result in drastically reduced transport rates of the test compounds. Moreover, the ancestral iridoid-producing leaf beetles already possess a fully functional import system for an early precursor of the iridoid defenses. Our data confirm an evolutionary scenario in which, after a host-plant change, the transport system of the leaf beetles may play a pivotal role in the adaptation on new hosts by selecting plant-derived glucosides that can be channeled to the defensive system.

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“…Given that the autogenous and host-derived defenses are quite dissimilar, the likelihood of such a convergent event might seem exceedingly low. However, chemical characterization of enzymes that are involved in the respective biogenetic routes indicates that the shift of defense might be because of a change in the specificity of an alcohol dehydrogenase (49,50), allowing the use of salicin as a new substrate for the enzyme. Hence, the iridoid and salicin metabolisms are probably mutually exclusive (unless there were gene duplication followed by functional diversification).…”

Section: Discussionmentioning

confidence: 99%

Feeding specialization and host-derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end

Termonia

Hsiao

Pasteels

et al. 2001

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

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Combination of molecular phylogenetic analyses of Chrysomelina beetles and chemical data of their defensive secretions indicate that two lineages independently developed, from an ancestral autogenous metabolism, an energetically efficient strategy that made the insect tightly dependent on the chemistry of the host plant. However, a lineage (the interrupta group) escaped this subordination through the development of a yet more derived mixed metabolism potentially compatible with a large number of new host-plant associations. Hence, these analyses on leaf beetles document a mechanism that can explain why high levels of specialization do not necessarily lead to ''evolutionary dead ends.''

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Biosynthesis of Defensive Allomones in Leaf Beetle Larvae: Stereochemistry of Salicylalcohol Oxidation in Phratora vitellinae and Comparison of Enzyme Substrate and Stereospecificity with Alcohol Oxidases from Several Iridoid Producing Leaf Beetles

Cited by 23 publications

References 13 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

Selective transport systems mediate sequestration of plant glucosides in leaf beetles: A molecular basis for adaptation and evolution

Feeding specialization and host-derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end

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