Herbivore Adaptations to Plant Cyanide Defenses

Ohlen, Maike van; Herfurth, Anna-Maria; Wittstock, Ute

doi:10.5772/66277

Cited by 12 publications

(20 citation statements)

References 145 publications

(259 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Tissue disruption brings these chemical defenses together with co-occurring β-glycosidases leading to their hydrolysis with subsequent release of toxic cyanide, e.g., into the gut lumen of a herbivore. The lack of correlation observed in [ 18 ] could be due to the presence of physiological and behavioural avoidance mechanisms in certain insect species such as Z. filipendulae in addition to detoxification capabilities (reviewed in [ 34 , 35 , 36 ]) and does not exclude a role of rhodaneses in cyanide detoxification. Our results prompt us to hypothesize that formation of cyanide as a consequence of xenobiotic metabolism in glucosinolate-feeding Pierinae (rather than plant-mediated breakdown of cyanogens) may require additional measures against cyanide poisoning which may include rhodaneses expressed in gut tissue.…”

Section: Discussionmentioning

confidence: 99%

β-Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation

Herfurth

Ohlen

Wittstock

2017

Insects

Self Cite

View full text Add to dashboard Cite

Cyanide is generated in larvae of the glucosinolate-specialist Pieris rapae (Lepidoptera:Pieridae) upon ingestion of plant material containing phenylalanine-derived glucosinolates as chemical defenses. As these glucosinolates were widespread within ancient Brassicales, the ability to detoxify cyanide may therefore have been essential for the host plant shift of Pierid species from Fabales to Brassicales species giving rise to the Pierinae subfamily. Previous research identified β-cyanoalanine and thiocyanate as products of cyanide detoxification in P. rapae larvae as well as three cDNAs encoding the β-cyanoalanine synthases PrBSAS1-PrBSAS3. Here, we analyzed a total of eight species of four lepidopteran families to test if their cyanide detoxification capacity correlates with their feeding specialization. We detected β-cyanoalanine synthase activity in gut protein extracts of all six species tested, which included Pierid species with glucosinolate-containing host plants, Pierids with other hosts, and other Lepidoptera with varying food specialization. Rhodanese activity was only scarcely detectable with the highest levels appearing in the two glucosinolate-feeding Pierids. We then amplified by polymerase chain reaction (PCR) 14 cDNAs encoding β-cyanoalanine synthases from seven species. Enzyme characterization and phylogenetic analysis indicated that lepidopterans are generally equipped with one PrBSAS2 homolog with high affinity for cyanide. A second β-cyanoalanine synthase which grouped with PrBSAS3 was restricted to Pierid species, while a third variant (i.e., homologs of PrBSAS1), was only present in members of the Pierinae subfamily. These results are in agreement with the hypothesis that the host shift to Brassicales was associated with the requirement for a specialized cyanide detoxification machinery.

show abstract

Section: Discussionmentioning

confidence: 99%

β-Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation

Herfurth

Ohlen

Wittstock

2017

Insects

Self Cite

View full text Add to dashboard Cite

show abstract

“…In arthropods the enzyme is present in a broad range of Lepidopteran species. This includes species containing CNglcs, such as Zygaenidae, but also acyanogenic species [ 78 , 79 ]. In the butterfly H. melpomone (Papilionoidea), β-cyanoalanine synthase activity is only present in feeding larval stages, corresponding to the developmental stages at which detoxification of ingested cyanogenic plant material is in demand [ 78 , 80 ].…”

Section: Detoxification Of Hcn Released From Cyanogenic Glucosidesmentioning

confidence: 99%

Cyanogenesis in Arthropods: From Chemical Warfare to Nuptial Gifts

Zagrobelny

Castro

Møller

et al. 2018

Insects

View full text Add to dashboard Cite

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...

show abstract

“…Plants also developed large spectra of anti-herbivore defences through the production of compounds of low molecular weight such as alkaloids, terpenes, glucosinolates, or cyanogenic glucosides (van Ohlen et al 2017). These chemical compounds may repel an enemy from a host plant or even harm the herbivore upon plant material ingestion (van Ohlen et al 2017, for reviews see Fürstenberg-Hägg et al 2013;War et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Dryas iulia (Lepidoptera, Nymphalidae) larval preference and performance on four sympatric Passiflora hosts

Arantes-Garcia¹,

Maia²,

Valadão³

et al. 2021

EuroJEcol

View full text Add to dashboard Cite

Host plant quality is determinant for herbivorous insects performance and survival. While on larval stages, insects select their host plants based on factors such as leaf nitrogen and water content, digestibility, and defences. Of great interest is the coevolutionary relationship between the Heliconiini insects and the Passiflora plants. In this study we experimentally evaluated Dryas iulia (Nymphalidae) larval preference to four sympatric Passiflora (Passifloraceae) and subsequently, the larval performance on the two most consumed species. We tested the hypothesis that D. iulia larvae prefer the Passiflora species with higher nutritional quality and lower defence, which supports the greatest larval performance. Dryas iulia larvae preferred P. misera (60.5% leaf consumption) over P. pohlii (28.9%), P. suberosa (15.5%), and P. edulis (not consumed). Passiflora misera presented the highest N concentration, third in water content, second in tector trichomes, and no glandular trichomes (only P. suberosa did). Nitrogen best explained D. iulia larvae leaf consumption; which further explains the greatest larval performance in P. misera than in P. suberosa: i.e. higher survival (23.1%), conversion efficiency of ingested food (32.8%), relative growth rate (14.8%), heavier pupae (15.2%), and lower relative consumption rate (13.8%). This study creates the opportunity to further investigate the Heliconiini-Passiflora system and showed that D. iulia larvae can assess and choose the host plant (even among sympatric species) that supports the greatest performance.

show abstract

Herbivore Adaptations to Plant Cyanide Defenses

Cited by 12 publications

References 145 publications

β-Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation

β-Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation

Cyanogenesis in Arthropods: From Chemical Warfare to Nuptial Gifts

Dryas iulia (Lepidoptera, Nymphalidae) larval preference and performance on four sympatric Passiflora hosts

Contact Info

Product

Resources

About