Flavin-Dependent Monooxygenases as a Detoxification Mechanism in Insects: New Insights from the Arctiids (Lepidoptera)

Sehlmeyer, Sven; Wang, Linzhu; Langel, Dorothee; Heckel, David G.; Mohagheghi, Hoda; Petschenka, Georg; Ober, Dietrich

doi:10.1371/journal.pone.0010435

Cited by 58 publications

(55 citation statements)

References 71 publications

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“…Sehlmeyer et al . () found the same enzyme in other PA‐feeding arctiid species and that the Lepidoptera has three gene families of flavin‐dependent monooxygenases. A gene duplication early in the arctiid lineage produced the pyrrolizidine‐alkaloid‐ N ‐oxygenase that enables these moths to feed on PA‐containing plants and to successfully accumulate these compounds in the tissue (Sehlmeyer et al .…”

Section: Introductionmentioning

confidence: 75%

A free lunch? No cost for acquiring defensive plant pyrrolizidine alkaloids in a specialist arctiid moth (Utetheisa ornatrix)

2012

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Many herbivorous insects sequester defensive chemicals from their host plants. We tested sequestration fitness costs in the specialist moth Utetheisa ornatrix (Lepidoptera: Arctiidae). We added pyrrolizidine alkaloids (PAs) to an artificial diet at different concentrations. Of all the larval and adult fitness components measured, only development time was negatively affected by PA concentration. These results were repeated under stressful laboratory conditions. On the other hand, the amount of PAs sequestered greatly increased with the diet PA concentration. Absence of a detectable negative effect does not necessarily imply a lack of costs if all individuals express the biochemical machinery of detoxification and sequestration constitutively. Therefore, we used qPCR to show that expression of the gene used to detoxify PAs, pyrrolizidine-alkaloid-N-oxygenase (pno), increased 41-fold in our highest PA treatment. Nevertheless, fitness components were affected only slightly or not at all, suggesting that sequestration in this species does not incur a strong cost. The apparent lack of costs has important implications for our understanding of the evolution of ecological interactions; for example, it implies that selection by specialist herbivores may decrease the levels of certain chemical defences in plant populations.

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Section: Introductionmentioning

confidence: 75%

A free lunch? No cost for acquiring defensive plant pyrrolizidine alkaloids in a specialist arctiid moth (Utetheisa ornatrix)

2012

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“…Although no analyses were performed to check if PAs are present only in the N-oxide form, we have made this assumption, since it has occurred in other arctiines studied. 3,4,15,16 The uptake of PA from plants may only occur in larvae of S. figulina, since we did not observe adults in PA sources.…”

Section: Discussionmentioning

confidence: 85%

“…1,2 However, specialized herbivores, such as arctiine moths, danaine and ithomiine butterflies and chrysomeline beetles, among others, are able to cope with pro-toxic free-base PAs from these plants, converting them into non-toxic N-oxides. 3,4 These insects sequester PA N-oxides, incorporating them into their tissues, and this renders chemical protection against predators and parasitoids. 1,5 Arctiine moths and danaine and ithomiine butterflies also use PAs as precursors of male sexual pheromones, such as the dihydropyrrolizine hydroxydanaidal.…”

Section: Introductionmentioning

confidence: 99%

Pyrrolizidine Alkaloids in the Pericopine MothScearctia figulina(Erebidae: Arctiinae): Metabolism and Chemical Defense

Martins

Trigo

2016

Journal of the Brazilian Chemical Society

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Pyrrolizidine alkaloids (PAs) are defensive compounds present in several plant families. However, some specialist herbivore insects have overcome these toxic compounds and sequester PAs converted to N-oxide as a defense against predators and a precursor of male sexual pheromones. In this context, we investigated PA sequestration by the specialist pericopine moth Scearctia figulina (Erebidae: Arctiinae), which feeds on leaves of Heliotropium transalpinum (Boraginaceae) as larvae. Additionally, we examined the role of PAs against different predators. The PAs sequestered from the host plant were metabolized by larvae and transferred to adults via two main pathways: (i) rinderine and its acetyl derivative (7S,3'R) were epimerized to intermedine (7R,3'R) and lycopsamine (7R,3'S), and (ii) insect PAs were biosynthesized from necine bases obtained from plant-acquired PAs, with necic acids of insect origin. Both metabolic products may be related to the biosynthesis of 7R male pheromone and to chemical defense. Larvae and adults were chemically protected against the spiders Nephila clavipes and Lycosa erythrognatha and the chick Gallus gallus, and this defense may be associated to PAs. Keywords: callimorphine, Heliotropium transalpinum, insect PAs, lycopsamine, predation IntroductionPyrrolizidine alkaloids, particularly 1,2-dehydropyrrolizidines (hereafter PAs), are powerful defensive compounds in several plant taxa, such as Eupatorieae and Senecioneae (Asteraceae), Boraginaceae, and Crotalarieae (Leguminosae).1,2 However, specialized herbivores, such as arctiine moths, danaine and ithomiine butterflies and chrysomeline beetles, among others, are able to cope with pro-toxic free-base PAs from these plants, converting them into non-toxic N-oxides.3,4 These insects sequester PA N-oxides, incorporating them into their tissues, and this renders chemical protection against predators and parasitoids.1,5 Arctiine moths and danaine and ithomiine butterflies also use PAs as precursors of male sexual pheromones, such as the dihydropyrrolizine hydroxydanaidal.6-8 PAs were also recorded in the grasshopper Zonocerus variegatus, the aphid Aphis jacobaeae, the bug Largus rufipennis, and the coccide Ceroplastes albolineatus.1 PA-containing insects are generally aposematic, i.e., their unpalatability is associated with warning signals alerting predators of this trait; warning signals can be visual, sonorous, or odorant. 9Among arctiine moths, 10 PAs were found in the tribes Amerilini and Arctiini (subtribes Callimorphina, Arctiina, Pericopina, Ctenuchina, Euchromiina, and Phaegopterina), but not in Lithosiini and Syntomini. 11 Three PA acquisition strategies were found in these moths: (i) PA-obtained as adults, (ii) PA-specialist feeding as larvae, and (iii) PA-generalist feeding as larvae.11 In the first syndrome, adults either feeding on nectar containing PAs or display a pharmacophagous behavior, or obtaining the alkaloid visiting withered PA-containing plants. 2,12,13 This syndrome was widely found in Ctenuchina, Euchromiina, an...

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“…Males with a higher load of PAs have been shown to be more attractive for females, a quality that is signaled by PA-derived courtship pheromones. A PA-specific enzyme, a PA N-oxygenase, enables this class of insects to store PAs in a polar protoxic form (39,40).…”

Section: Discussionmentioning

confidence: 99%

New aspect of plant–rhizobia interaction: Alkaloid biosynthesis in Crotalaria depends on nodulation

Irmer

Podzun

Langel

et al. 2015

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

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Infection of legume hosts by rhizobial bacteria results in the formation of a specialized organ, the nodule, in which atmospheric nitrogen is reduced to ammonia. Nodulation requires the reprogramming of the plant cell, allowing the microsymbiont to enter the plant tissue in a highly controlled manner. We have found that, in Crotalaria (Fabaceae), this reprogramming is associated with the biosynthesis of pyrrolizidine alkaloids (PAs). These compounds are part of the plant’s chemical defense against herbivores and cannot be regarded as being functionally involved in the symbiosis. PAs in Crotalaria are detectable only when the plants form nodules after infection with their rhizobial partner. The identification of a plant-derived sequence encoding homospermidine synthase (HSS), the first pathway-specific enzyme of PA biosynthesis, suggests that the plant and not the microbiont is the producer of PAs. Transcripts of HSS are detectable exclusively in the nodules, the tissue with the highest concentration of PAs, indicating that PA biosynthesis is restricted to the nodules and that the nodules are the source from which the alkaloids are transported to the above ground parts of the plant. The link between nodulation and the biosynthesis of nitrogen-containing alkaloids in Crotalaria highlights a further facet of the effect of symbiosis with rhizobia on the ecologically important trait of the plant’s chemical defense.

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Flavin-Dependent Monooxygenases as a Detoxification Mechanism in Insects: New Insights from the Arctiids (Lepidoptera)

Cited by 58 publications

References 71 publications

A free lunch? No cost for acquiring defensive plant pyrrolizidine alkaloids in a specialist arctiid moth (Utetheisa ornatrix)

A free lunch? No cost for acquiring defensive plant pyrrolizidine alkaloids in a specialist arctiid moth (Utetheisa ornatrix)

Pyrrolizidine Alkaloids in the Pericopine MothScearctia figulina(Erebidae: Arctiinae): Metabolism and Chemical Defense

New aspect of plant–rhizobia interaction: Alkaloid biosynthesis in Crotalaria depends on nodulation

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