Cyanogenesis in Arthropods: From Chemical Warfare to Nuptial Gifts

Abstract

Chemical defences are key components in insect–plant interactions, as insects continuously learn to overcome plant defence systems by, e.g., detoxification, excretion or sequestration. Cyanogenic glucosides are natural products widespread in the plant kingdom, and also known to be present in arthropods. They are stabilised by a glucoside linkage, which is hydrolysed by the action of β-glucosidase enzymes, resulting in the release of toxic hydrogen cyanide and deterrent aldehydes or ketones. Such a binary system of components that are chemically inert when spatially separated provides an immediate defence against predators that cause tissue damage. Further roles in nitrogen metabolism and inter- and intraspecific communication has also been suggested for cyanogenic glucosides. In arthropods, cyanogenic glucosides are found in millipedes, centipedes, mites, beetles and bugs, and particularly within butterflies and moths. Cyanogenic glucosides may be even more widespread since many arthropod taxa have not yet been analysed for the presence of this class of natural products. In many instances, arthropods sequester cyanogenic glucosides or their precursors from food plants, thereby avoiding the demand for de novo biosynthesis and minimising the energy spent for defence. Nevertheless, several species of butterflies, moths and millipedes have been shown to biosynthesise cyanogenic glucosides de novo, and even more species have been hypothesised to do so. As for higher plant species, the specific steps in the pathway is catalysed by three enzymes, two cytochromes P450, a glycosyl transferase, and a general P450 oxidoreductase providing electrons to the P450s. The pathway for biosynthesis of cyanogenic glucosides in arthropods has most likely been assembled by recruitment of enzymes, which could most easily be adapted to acquire the required catalytic properties for manufacturing these compounds. The scattered phylogenetic distribution of cyanogenic glucosides in arthropods indicates that the ability to biosynthesise this class of natural products has evolved independently several times. This is corroborated by the characterised enzymes from the pathway in moths and millipedes. Since the biosynthetic pathway is hypothesised to have evolved convergently in plants as well, this would suggest that there is only one universal series of unique intermediates by which amino acids are efficiently converted into CNglcs in different Kingdoms of Life. For arthropods to handle ingestion of cyanogenic glucosides, an effective detoxification system is required. In butterflies and moths, hydrogen cyanide released from hydrolysis of cyanogenic glucosides is mainly detoxified by β-cyanoalanine synthase, while other arthropods use the enzyme rhodanese. The storage of cyanogenic glucosides and spatially separated hydrolytic enzymes (β-glucosidases and α-hydroxynitrile lyases) are important for an effective hydrogen cyanide release for defensive purposes. Accordingly, such hydrolytic enzymes are also present in many cyanogenic arthropods, an...

Sequestration and biosynthesis of cyanogenic glucosides in passion vine butterflies and consequences for the diversification of their host plants

“…Whereas sequestration of cyclopentenyl CNglcs has been reported only in butterflies of the Heliconiinae subfamily, biosynthesis of linamarin and lotaustralin has been demonstrated in several species of butterflies and moths belonging to many taxonomically distinct families, such as Zygaenidae, Limacodidae, Heterogynidae, Nymphalidae, and Lycaenidae (Davis & Nahrstedt, ; Nahrstedt, ; Zagrobelny, Castro et al, ). The biosynthetic pathway in the burnet moth Z. filipendulae is encoded by the genes ZfCYP405A2 , ZfCYP332A3, and ZfUGT33A1 (Jensen et al, ) and putative homologues of these P450s have been found in the genome of the postman butterfly H. melpomene, HmCYP405A4 , HmCYP405A5, HmCYP405A6, and HmCYP332A1 (Chauhan et al, ) and in other Heliconius species (Zagrobelny, Jensen, Vogel, Feyereisen, & Bak, ).…”

“…Similar to H. sapho , all species of the sara‐sapho group feeding on Astrophea plants contain only epivolkenin, and it is possible that they may have lost the ability to synthesize aliphatic CNglcs to become more specialized in sequestration as suggested by Engler‐Chaouat and Gilbert (). Yet, apparently functional P450 genes associated with the biosynthesis of linamarin and lotaustralin are present in the genome of H. sapho (Zagrobelny, Castro et al, ) suggesting that the lack of biosynthesis could be due to transcriptional and/or translational mechanisms. On the other hand, large amounts of linamarin and lotaustralin were found in H. sara and H. charithonia which, although belonging to the same group as H. sapho , are not Astrophea specialists but Decaloba specialists .…”

“…Although the pathways in plants and insects share the same catalytic reactions and enzyme types, the genes encoding the enzymes are not orthologues, confirming that the ability to produce aliphatic CNglcs arose independently in these two Kingdoms. Heliconiine butterflies also synthesize the aliphatic CNglcs linamarin and lotaustralin through the same enzymatic steps as Zygaena (Davis & Nahrstedt, ), and genes homologous to ZfCYP405A2 and ZfCYP332A3 have been found in the H. melpomene genome (Chauhan, Jones, Wilkinson, Pauchet, & ffrench‐Constant, ) and other Heliconius species (Zagrobelny, Castro et al, ) although, they have not yet been functionally characterized. This indicates that the biosynthetic pathway of linamarin and lotaustralin has originated in a common ancestor of butterflies and moths (Zagrobelny, Castro et al, ).…”

Variation of chemical compounds in wild Heliconiini reveals ecological factors involved in the evolution of chemical defenses in mimetic butterflies

“…Larvae of most Heliconiini species synthesize CGs de novo (Wray, Davis, & Nahrstedt, ), but many sequester CGs from the host plants (Engler et al, ). Both synthesis and sequestration of CGs are only observed in Zygaenidae (burnet moths) and Heliconiini, two clades where aposematic color patterns have evolved (Zagrobelny, Castro, Møller, & Bak, ). So far, Heliconiini have been reported to sequester five cyclopentenoid CGs from Passiflora ; the diastereoisomers tetraphyllin B and epivolkenin, tetraphyllin A, gynocardin, and dihydrogynocardin (Figure ) (Castro, Zagrobelny, et al, ; Engler et al, ).…”

“…Larvae of most Heliconiini species synthesize CGs de novo (Wray, Davis, & Nahrstedt, 1983), but many sequester CGs from the host plants (Engler et al, 2000). Both synthesis and sequestration of CGs are only observed in Zygaenidae (burnet moths) and Heliconiini, two clades where aposematic color patterns have evolved (Zagrobelny, Castro, Møller, & Bak, 2018).…”