Lepidopteran defence droplets - a composite physical and chemical weapon against potential predators

Pentzold, Stefan; Zagrobelny, Mika; Khakimov, Bekzod; Engelsen, Søren Balling; Clausen, Henrik; Petersen, Bent Larsen; Borch, Jonas; Møller, Birger Lindberg; Bak, Søren

doi:10.1038/srep22407

Cited by 18 publications

(35 citation statements)

References 61 publications

(98 reference statements)

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“…The ingested non-SMC cyanogens might be degraded by b-glucosidases and ahydroxynitrile lyases (Zagrobelny et al 2004;Ketudat Cairns & Esen 2010). Although no specific b-glucosidase involved in CNglc catabolism has been characterized in insects yet, a b-glucosidase (ZfBGD1) has been identified in CNglc-containing droplets of Zygaena filipendulae larvae (Pentzold et al 2016). Among the 326 DEGs in the H. melpomene gut after host plant shift, three homologs of b-glucosidase enzymes (HMEL013290, HMEL014474 and HMEL014483) were identified.…”

Section: Differentially Expressed Genesmentioning

confidence: 99%

The transcriptome response of Heliconius melpomene larvae to a novel host plant

Fang

Zhang

et al. 2016

Molecular Ecology

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In the warfare between herbivore and host plant, insects have evolved a variety of defensive mechanisms, including allelochemical transformation and excretion. Several studies have explored the transcriptome responses of insects after host plant shifts to understand these mechanisms. We investigated the plastic responses of Heliconius melpomene larvae feeding on a native host Passiflora menispermifolia and a less strongly defended nonhost species, Passiflora biflora. In total, 326 differentially expressed genes were identified, with a greater number upregulated on the more strongly defended native host. Functional annotation showed that detoxifying enzymes, transporters and components of peritrophic membrane were strongly represented. In total, 30 candidate detoxification genes were differentially expressed, with glutathione S-transferases (GSTs) and UDP-glucuronosyltransferases (UGTs) showing the highest proportion of differential expression, 27.3% and 17.3%, respectively. These differentially expressed detoxification genes were shown to evolve mainly under the influence of purifying selection, suggesting that protein-coding evolution has not played a major role in host adaptation. We found only one gene, GSTe3, with evidence of adaptive evolution at H40, which is around the G-site and might alter enzyme activity. Based on our transcriptome and molecular evolution analysis, we suggest that transcriptional plasticity of genes in a herbivore may play an important role in adaptation to a new host plant.

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Section: Differentially Expressed Genesmentioning

confidence: 99%

The transcriptome response of Heliconius melpomene larvae to a novel host plant

Fang

Zhang

et al. 2016

Molecular Ecology

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“…This is because the only β-glucosidase present in the defence droplets (ZfBGD1) cannot hydrolyse linamarin and lotaustralin [29]. However, in case of severe injury of a larva, CNglcs in the droplets will come in contact with exuding haemolymph and thus mix with the ZfBGD2 enzyme identified in this study.…”

Section: Discussionmentioning

confidence: 90%

“…PCR amplification of the open reading frames were carried out as in [29]. For primers used, see electronic supplementary material, table S1.…”

Section: Methodsmentioning

confidence: 99%

Spatial separation of the cyanogenic β-glucosidase ZfBGD2 and cyanogenic glucosides in the haemolymph ofZygaenalarvae facilitates cyanide release

et al. 2017

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Low molecular weight compounds are typically used by insects and plants for defence against predators. They are often stored as inactive β-glucosides and kept separate from activating β-glucosidases. When the two components are mixed, the β-glucosides are hydrolysed releasing toxic aglucones. Cyanogenic plants contain cyanogenic glucosides and release hydrogen cyanide due to such a well-characterized two-component system. Some arthropods are also cyanogenic, but comparatively little is known about their system. Here, we identify a specific β-glucosidase (ZfBGD2) involved in cyanogenesis from larvae of Zygaena filipendulae (Lepidoptera, Zygaenidae), and analyse the spatial organization of cyanide release in this specialized insect. High levels of ZfBGD2 mRNA and protein were found in haemocytes by transcriptomic and proteomic profiling. Heterologous expression in insect cells showed that ZfBGD2 hydrolyses linamarin and lotaustralin, the two cyanogenic glucosides present in Z. filipendulae. Linamarin and lotaustralin as well as cyanide release were found exclusively in the haemoplasma. Phylogenetic analyses revealed that ZfBGD2 clusters with other insect β-glucosidases, and correspondingly, the ability to hydrolyse cyanogenic glucosides catalysed by a specific β-glucosidase evolved convergently in insects and plants. The spatial separation of the β-glucosidase ZfBGD2 and its cyanogenic substrates within the haemolymph provides the basis for cyanide release in Z. filipendulae. This spatial separation is similar to the compartmentalization of the two components found in cyanogenic plant species, and illustrates one similarity in cyanide-based defence in these two kingdoms of life.

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“…; Pentzold et al. , ). Prior to LC‐MS analysis, the frozen samples were each ground up in 1ml ice‐cold 55% MeOH, containing 0.1% formic acid and 0.044 mM amygdalin, a cyanogenic glucoside not found in the Zygaenidae, as an internal standard.…”

Section: Methodsmentioning

confidence: 98%

Sex differences but no evidence of quantitative honesty in the warning signals of six-spot burnet moths (Zygaena filipendulaeL.)*

et al. 2018

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The distinctive black and red wing pattern of six‐spot burnet moths (Zygaena filipendulae, L.) is a classic example of aposematism, advertising their potent cyanide‐based defences. While such warning signals provide a qualitatively honest signal of unprofitability, the evidence for quantitative honesty, whereby variation in visual traits could provide accurate estimates of individual toxicity, is more equivocal. Combining measures of cyanogenic glucoside content and wing color from the perspective of avian predators, we investigate the relationship between coloration and defences in Z. filipendulae, to test signal honesty both within and across populations. There were no significant relationships between mean cyanogenic glucoside concentration and metrics of wing coloration across populations in males, yet in females higher cyanogenic glucoside levels were associated with smaller and lighter red forewing markings. Trends within populations were similarly inconsistent with quantitative honesty, and persistent differences between the sexes were apparent: larger females, carrying a greater total cyanogenic glucoside load, displayed larger but less conspicuous markings than smaller males, according to several color metrics. The overall high aversiveness of cyanogenic glucosides and fluctuations in color and toxin levels during an individual's lifetime may contribute to these results, highlighting generally important reasons why signal honesty should not always be expected in aposematic species.

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Lepidopteran defence droplets - a composite physical and chemical weapon against potential predators

Cited by 18 publications

References 61 publications

The transcriptome response of Heliconius melpomene larvae to a novel host plant

The transcriptome response of Heliconius melpomene larvae to a novel host plant

Spatial separation of the cyanogenic β-glucosidase ZfBGD2 and cyanogenic glucosides in the haemolymph ofZygaenalarvae facilitates cyanide release

Sex differences but no evidence of quantitative honesty in the warning signals of six-spot burnet moths (Zygaena filipendulaeL.)*

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