Metabolism, excretion and avoidance of cyanogenic glucosides in insects with different feeding specialisations

Pentzold, Stefan; Zagrobelny, Mika; Bjarnholt, Nanna; Kroymann, Juergen; Vogel, Heiko; Olsen, Carl Erik; Møller, Birger Lindberg; Bak, Søren

doi:10.1016/j.ibmb.2015.10.004

Cited by 32 publications

(31 citation statements)

References 63 publications

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“…Prunasin is not naturally present in the food plant of Z. filipendulae larvae, but it can be sequestered by them [57], and may be ingested from food plants by other species of Zygaenidae (Chiharu Koshio 2016, personal communication). Only few insect GH1 β-glucosidases involved in chemical defence have been functionally characterized: a myrosinase from the striped flea beetle P. striolata hydrolysing sequestered aliphatic glucosinolates [10], and a β-glucosidase from glands in juvenile Chrysomelina leaf beetles hydrolysing e.g.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…; 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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“…The nitrile-specifier protein in the gut of P. rapae blocks the formation of glucosinolate hydrolysis products to form simple nitriles that are then excreted with the frass (Wittstock et al, 2004;Pentzold et al, 2015). The turnip sawfly uses a different approach: it is able to overcome the glucosinolate-myrosinase system by sequestering intact glucosinolates in the hemolymph and the sequestered glucosinolates are then used to deter larval predators (Müller et al, 2001).…”

Section: Chapter 5 General Discussionmentioning

confidence: 99%

“…The next step is to determine the specific mechanism used by C. pavonana to circumvent this toxicity using molecular and analytical techniques (e.g. Schramm et al, 2012;Pentzold et al, 2015). In addition, to further study the role of plant/leaf age and the effect of the morphological characteristics brought about by plant ageing on the feeding behaviour of C. pavonana, future experiments should use plant ages that cover a large span of the cabbage plants life cycle.…”

Section: Chapter 5 General Discussionmentioning

confidence: 99%

“…Despite the ability of plants to build up defense compounds to protect themselves from subsequent herbivore attacks (Ahuja et al, 2010;Schramm et al, 2011;Mewis et al, 2005;Shroff et al, 2008;Falk and Gershenzon, 2007), some generalist and specialist feeders have developed strategies to overcome toxicity or countermeasures which enable them to feed successfully with little or no adverse effects on their growth, development and survival (Wittstock et al, 2004;Falk and Gershenzon, 2007;Textor and Gershenzon, 2009;Winde & Wittstock, 2011;Schramm et al, 2011;Heckel, 2014;Pentzold et al, 2015). Some insect species have incorporated plants containing glucosinolate into their diets (Falk and Gershenzon, 2007) by modifying physiological processes that result in evasion of the toxins (Brattsten, 1992).…”

Section: Figure 12mentioning

confidence: 99%

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Choice of feeding sites, growth and survival by Crocidolomia pavonana (F.)

Tadle¹

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The large cabbage moth, Crocidolomia pavonana (F.) (Lepidoptera: Crambidae), is one of the most significant pests of Brassica crops and has re-emerged as a serious pest of crucifer crops in tropical and sub-tropical Asia because of the control used against the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). The damage caused by this pest can be significant because larvae devour young tissues of the plant at different stages and bore into the centre of the cabbage head at maturity and can damage the whole cabbage plant. Despite its economic importance the interaction of this pest with its host plant is not well understood.The current study showed that larval feeding by C. pavonana was influenced by the presence of cabbage in artificial diet, in laboratory bioassays. Of the four diets developed and tested, neonates survived and completed developmental stages (81%) on diet containing cabbage (Brassica oleracea cv sugarloaf) more so than on base diet (diet without cabbage), diet containing wheat grass or spinach powder. Neonates were able to locate diet with cabbage powder but not when cabbage was absent (i.e. base diet).Similarly, in an olfactometer test, neonates were strongly attracted to the odour of diet with cabbage compared with diet without cabbage. More than twice the number of feeding events was observed on filter paper disks impregnated with diet containing cabbage powder than on paper disks with base diet. The behavioural responses of neonates to diet with cabbage are linked to the glucosinolates present on cabbage plants. Sinigrin elicited feeding when added to diet without cabbage and also when applied to a non-host plant, Gossypium hirsutum (Sicot 71RRF). Neonates' response to allyl isothiocyanate in a twoarm olfactometer was stronger than to sinigrin, which would explain larval attraction to damaged cabbage plants. These results indicate that sinigrin and allyl isothiocyanate provide important feeding and olfactory cues for C. pavonana larvae.Larval feeding and moth oviposition behaviour of C. pavonana was further studied using whole cabbage plants of two different ages (6 and 8-leaf stage) and this was compared to the response of a well-studied crucifer specialist, P. xylostella. Plant age did not significantly affect oviposition and feeding preference by C. pavonana whereas P. xylostella preferred younger plants for oviposition and larval feeding. The intra-plant distribution of eggs and feeding sites was similar for both species, but egg distribution showed a pattern different from feeding sites. Neonates that hatched from eggs deposited ii on lower leaves moved towards the apical portion of the plant and established a majority of feeding sites on younger leaves. Preference for younger leaves was also observed on excised leaves, indicating architectural position was not the factor driving choice. Younger leaves are known to have a higher concentration of nitrogen content and proteins suitable for larval development, whereas lower leaves are considered not palatable b...

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Metabolism, excretion and avoidance of cyanogenic glucosides in insects with different feeding specialisations

Cited by 32 publications

References 63 publications

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

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.)*

Choice of feeding sites, growth and survival by Crocidolomia pavonana (F.)

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