Characterization of an extracellular salicyl alcohol oxidase from larval defensive secretions of Chrysomela populi and Phratora vitellinae (Chrysomelina)

Brückmann, Markus; Termonia, Arnaud; Pasteels, Jacques; Hartmann, Thomas

doi:10.1016/s0965-1748(02)00072-3

Cited by 32 publications

(41 citation statements)

References 22 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%

“…These SAOs belong to the glucose-methanol-choline (GMC) oxidoreductase multi-gene family [22,23] and convert salicyl alcohol into salicylaldehyde [20]. Comparative genome analyses show that the GMC oxidoreductase family harbours genes, most of which are in a cluster and unique with respect to their expansion in insects [24][25][26].…”

Section: Introductionmentioning

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]. However, the recombinant SAO from the salicylaldehyde-producing Ph.…”

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%

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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“…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%

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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“…In reservoirs of defence glands, salicin is hydrolyzed to salicyl alcohol saligenin. Salicylaldehyde which is the main defence compound against predators and parasitoids originates through its oxidation (Brückmann et al 2002). The production of salicylaldehyde by larvae of C. populi on poplars is also mentioned by Matsuda and Sugawara (1980), Pasteels et al (1988), etc.…”

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confidence: 99%

Occurrence, bionomics and harmfulness of Chrysomela populi L. (Coleoptera, Chrysomelidae)

Urban¹

2006

J. For. Sci.

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ABSTRACT:In 2003 to 2005, Chrysomela populi L. gradated on yearly cut Populus nigra var. italica in street alleys in Brno and elsewhere. Imagoes occurred on trees from the end of April or from the beginning of May. In rearing, the chrysomelid consumed unwillingly leaves of 2-year shoots and laid on average 142 eggs. On leaves of shoots, imagoes damaged 100 to 200 cm 2 during 5 to 7 weeks, produced 480 to 900 frass pellets and laid on average 506 eggs. Oviposition was continual with breaks amounting to on average 2.6 days. Embryonal development took 6 to 8 (in the laboratory 5) days. Larvae of the 1 st generation occurred from mid-May to mid-July. In the course of 2 weeks (in the laboratory during 10 days) of life, they damaged about 20 cm 2 leaves and produced about 300 frass pallets. In the laboratory, prepupae took 2 days and pupae 4 days. Imagoes of the 1 st generation occurred from June to September. They damaged on average 113 cm 2 and produced on average 553 frass pellets and 653 eggs. At a temperature of 24 to 28°C, imagoes damaged on average 84 cm 2 during 2 to 3 weeks and diapaused until the next year. On growing up leaves, imagoes lived longer showing higher consumption of food and higher fecundity as against new fully-grown leaves. Larvae of the 2 nd generation destroyed on average 2 cm 2 smaller area than larvae of the 1 st generation. Part or all imagoes of the 2 nd generation diapaused. Imagoes of the 3 rd generation damaged 40 to 70 cm 2 leaves before departure to wintering grounds. In our natural conditions, the prospective 3 rd generation is always incomplete. Cleonice callida Meig. and Schizonotus sieboldi (Ratz.) rank among important enemies.

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Characterization of an extracellular salicyl alcohol oxidase from larval defensive secretions of Chrysomela populi and Phratora vitellinae (Chrysomelina)

Cited by 32 publications

References 22 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

Occurrence, bionomics and harmfulness of Chrysomela populi L. (Coleoptera, Chrysomelidae)

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